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(Radiology. 2000;214:678-682.)
© RSNA, 2000


Neuroradiology

MR Angiography of the Intracranial Venous System1

Lishya Liauw, MD, Mark A. van Buchem, MD, PhD, Aart Spilt, MD, Francisca T. de Bruïne, MD, René van den Berg, MD, Jo Hermans, PhD and Martin N. J. M. Wasser, MD, PhD

1 From the Departments of Radiology (L.L., M.A.v.B., A.S., F.T.d.B., R.v.d.B., M.N.J.M.W.) and Medical Statistics (J.H.), Leiden University Medical Center, PO Box 9600, 2300 RC Leiden, the Netherlands. Received March 1, 1999; revision requested April 26; revision received June 25; accepted August 2. Address reprint requests to L.L.


    Abstract
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To compare the effectiveness of different imaging planes at time-of-flight (TOF) magnetic resonance (MR) angiography and phase-contrast MR angiography in the visualization of the normal intracranial venous system.

MATERIALS AND METHODS: In 12 healthy volunteers, two-dimensional (2D) TOF MR angiography and three-dimensional (3D) phase-contrast MR angiography were performed in transverse, sagittal, and coronal planes. All data were displayed as maximum intensity projection (MIP) images. Four neuroradiologists assessed the visibility of 28 intracranial venous structures on the MIP images. Statistical analysis was performed by using the Friedman two-way analysis of variance and the Cochran Q test.

RESULTS: Visualization of the normal intracranial venous system was better with 3D phase-contrast and coronal 2D TOF MR angiography than with transverse or sagittal 2D TOF MR angiography (P < .05, Friedman test) for each observer and the group of observers. Differences were found between each of the 2D TOF and 3D phase-contrast MR angiographic sequences in the visualization of individual venous structures (Cochran Q test). The {kappa} values ranged from 0.36 to 0.71, which indicated a moderate to good agreement between observers.

CONCLUSION: The normal intracranial venous system is adequately visualized with 3D phase-contrast and coronal 2D TOF MR angiography.

Index terms: Cerebral blood vessels, MR, 176.12142, 177.12142, 176.91, 177.91 • Magnetic resonance (MR), angiography, 176.12142, 177.12142 • Magnetic resonance (MR), comparative studies, 176.12142, 177.12142 • Magnetic resonance (MR), maximum intensity projection, 176.12142, 177.12142 • Magnetic resonance (MR), phase imaging, 176.12142, 177.12142 • Magnetic resonance (MR), three-dimensional, 176.12142, 177.12142 • Magnetic resonance (MR), time of flight, 176.12142, 177.12142


    Introduction
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The intracranial venous system is a complex three-dimensional (3D) structure with a variable and often asymmetric anatomy (1). Visualization of the intracranial venous system is important in a number of clinical situations, such as the diagnosis of intracranial venous thrombosis and the preoperative assessment of the patency of dural sinus lumina encased by meningioma. Over the years, several imaging techniques have been used to visualize the intracranial venous system. Even after the introduction of computed tomography, conventional cerebral angiography was the standard for a long time.

However, with the advent of magnetic resonance (MR) imaging and, in particular, after the introduction of MR angiographic techniques, it became possible to visualize the intracranial venous system without the use of invasive procedures or ionizing irradiation. In addition, contrary to conventional angiography, MR angiography can be used to distinguish occlusion from agenesis of a venous structure. Nowadays, MR imaging and MR angiography is considered the modality of choice for imaging the venous cerebral system (29). From a review of the literature, however, it is not clear which of the available MR angiographic techniques is best suited for this purpose, since formal comparisons of the techniques are lacking.

Furthermore, for the optimization of an MR angiographic protocol, it is important to adapt the imaging plane to the direction of flow. Since blood flows in many planes and directions in the intracranial venous system, it is not clear before imaging which plane is optimal for MR angiography. To our knowledge, the effect of the imaging plane on the visibility of the intracranial venous system was assessed in only one study (10); in that study, only time-of-flight (TOF) techniques and only two of the three standard imaging planes were investigated.

The aim of our study was to compare TOF and phase-contrast MR angiography in three standard orientations in the visualization of the normal intracranial venous system. The results of this study may help to guide future studies in which TOF MR angiography and phase-contrast MR angiography are compared in the diagnosis of intracranial venous disease.


    MATERIALS AND METHODS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Our study included a total of 26 volunteers (15 men, 11 women; age range, 23–54 years; mean age, 32 years). First, we obtained flow measurements to select the optimal velocity encoding, or Venc, for the phase-contrast MR angiographic technique to be used thereafter. In 11 healthy volunteers (six men, five women; age range, 23–54 years; mean age, 37 years) flow measurements were obtained by using a two-dimensional (2D) cine phase-contrast MR angiographic technique (15/8.5 [repetition time msec/echo time msec], 20° flip angle, 6-mm section thickness, four signals acquired) in the superior sagittal sinus, straight sinus, and both transverse sinuses at 0.5 T.

Flow in the superior sagittal sinus was measured anteriorly and posteriorly at a point 1 cm cranial to the confluence of sinuses. Flow in the transverse sinus was measured at a point 1 cm distal to the confluence of sinuses. In the straight sinus, flow was measured halfway between the origin and the end of the straight sinus. For the assessment of flow velocities, we used an automated method to quantify flow (11). In the complete cross sections of these vessels, we quantified the average flow during one cardiac cycle. In these 11 volunteers, we measured a large range of flow velocities (Table 1).


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TABLE 1. Flow Velocities Measured in the Dural Sinuses with an Automated Method to Quantify Flow
 
To avoid aliasing, the measured maximum averaged flow is two-thirds of the optimal velocity encoding for phase-contrast MR angiography. According to this, the velocity encoding should have been 13 cm/sec (9.19 cm/sec ÷ 0.7, where 9.19 is the highest flow velocity measured [Table 1]). However, because of the range of flow velocities we observed, it was not possible to select a velocity encoding that was optimal for each venous structure in each individual. We chose a velocity encoding of 15 cm/sec, which was higher than 13 cm/sec, to minimize the risk of aliasing. By using this velocity encoding phase-contrast MR angiography was sensitive to the flow in small vessels and lacked aliasing in the larger venous structures such as the transverse sinus. By using a higher velocity encoding, phase-contrast MR angiography became insensitive to the flow in small veins.

Second, in a pilot study, we performed 2D phase-contrast MR angiography, 3D phase-contrast MR angiography, 2D TOF MR angiography, and 3D TOF MR angiography in the transverse plane in three additional healthy volunteers (two men, one woman; age range, 28–34 years; mean age, 30 years), to assess whether the 2D or 3D technique would enable better qualitative visualization of the normal intracranial venous system. (Parameters used in each sequence appear in Table 2.)


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TABLE 2. Parameters for MR Angiographic Sequences
 
For 2D and 3D phase-contrast MR angiography, arterial presaturation was used. For 3D phase-contrast MR angiography, three directions of flow encoding were used with an identical velocity encoding in all directions. Two-dimensional phase-contrast MR angiography and 3D TOF MR angiography were considered unsuitable for the visualization of the normal intracranial venous system. At 2D phase-contrast MR angiography, a marked intravascular signal loss was found because of the larger voxel size, which resulted in increased intravoxel dephasing. Large parts of the intracranial venous system were not visualized at 3D TOF MR angiography because of severe in-plane saturation. Three-dimensional phase-contrast MR angiography and 2D TOF MR angiography clearly enabled the best visualization.

Third, the two MR angiographic techniques we selected from the pilot study (3D phase-contrast MR angiography and 2D TOF MR angiography) were applied in 12 additional healthy volunteers (seven men, five women; age range, 23–37 years; mean age, 29 years) to compare the visualization of the intracranial venous system. Each pulse sequence was applied in three standard orientations (transverse, coronal, and sagittal) to study the effect on the visibility of the intracranial venous system. This resulted in the use of six MR angiographic sequences per volunteer. We used an MR imaging system (ACS NT 15; Philips Medical Systems, Best, the Netherlands) that operated at a field strength of 1.5 T.

All data were displayed as maximum intensity projection (MIP) images. Three MIP images were generated per sequence: We generated two transverse MIP images, a rostral one that depicted the cortical veins (without superimposition of the deep venous system) and a caudal one that depicted the deep venous system (without superimposition of the cortical veins). We also generated a sagittal MIP image, which consisted of a midsagittal section for the visualization of the deep venous system (without superimposition of lateral structures).

Four neuroradiologists (L.L., F.T.d.B., R.v.d.B., M.A.v.B.) independently assessed the visibility of the 28 predefined intracranial venous structures on the MIP images obtained with each sequence (Table 3). The three MIP images obtained with the same sequence were presented together. The observers were blinded to the sequence used. Visibility was scored as complete or incomplete (including no visibility).


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TABLE 3. Frequency of Complete Visualization of the 28 Intracranial Venous Structures with each MR Angiographic Sequence
 
Subsequently, for each observer, we assessed how often each venous structure was completely visible to each observer with each sequence in the 12 volunteers. Thus, the maximal score per structure was 48. The combined scores of all venous structures per sequence gave an impression of the visibility of the intracranial venous system (maximal score = 28 x 48). Because we did not have a standard for the presence of veins in these healthy volunteers, we were unable to provide the sensitivity and specificity. Instead, we compared the MR angiographic sequences in terms of technique (TOF or phase-contrast) and orientation of the imaging plane.

Statistical analysis was performed by using the Friedman two-way analysis of variance and the Cochran Q test to compare the visualization of each of the 28 predefined structures with the six sequences. The Friedman test was used to assess which sequence or sequences allowed the best visualization of all 28 structures. The Cochran Q test was used to identify subsets of structures for which another sequence was better than the best sequence determined by the results of the Friedman test. A {kappa} statistic was calculated to measure the agreement between the four observers. For all statistical analysis, a P value of < .05 was considered to indicate a significant difference. We had review board approval for our study, and we obtained informed consent from the volunteers.


    RESULTS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Table 3 shows the frequencies with which each of the 28 predefined structures were completely visible per MR angiographic sequence. Data for the four observers and 12 volunteers were taken together; therefore, the maximal frequency with which each structure was visible in each of the six MR angiographic sequences was 48. The intracranial venous system was better visualized with the three 3D phase-contrast MR angiographic sequences and the coronal 2D TOF sequence than with the sagittal or transverse 2D TOF sequence (P < .05, Friedman test) (Figs 1, 2; Table 4).



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Figure 1a. Transverse MIP images obtained with (a) sagittal and (b) transverse 2D TOF MR angiographic sequences (26/11, 50° flip angle) in the same volunteer. Note the decreased visibility of the left and right (arrowheads in b) transverse sinuses due to in-plane saturation. Also note the right (straight arrow in a) and left (straight arrow in b) sigmoid sinuses and the left (curved arrow in a) and right (curved arrow in b) basal veins of Rosenthal. In a, the imaging plane is perpendicular to the flow in the transverse sinuses, which limits in-plane saturation.

 


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Figure 1b. Transverse MIP images obtained with (a) sagittal and (b) transverse 2D TOF MR angiographic sequences (26/11, 50° flip angle) in the same volunteer. Note the decreased visibility of the left and right (arrowheads in b) transverse sinuses due to in-plane saturation. Also note the right (straight arrow in a) and left (straight arrow in b) sigmoid sinuses and the left (curved arrow in a) and right (curved arrow in b) basal veins of Rosenthal. In a, the imaging plane is perpendicular to the flow in the transverse sinuses, which limits in-plane saturation.

 


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Figure 2a. Sagittal MIP images obtained with (a) coronal and (b) sagittal 3D phase-contrast MR angiographic sequences (27/12, 20° flip angle) in the same volunteer. Note the similar depiction of the venous structures, including the basal veins of Rosenthal (straight solid arrow), the internal cerebral veins (curved solid arrow), the straight sinus (straight open arrow), and the superior sagittal sinus (arrowhead). The imaging plane (coronal, transverse, or sagittal) affects the visibility of the venous system at 2D TOF MR angiography but not at 3D phase-contrast MR angiography.

 


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Figure 2b. Sagittal MIP images obtained with (a) coronal and (b) sagittal 3D phase-contrast MR angiographic sequences (27/12, 20° flip angle) in the same volunteer. Note the similar depiction of the venous structures, including the basal veins of Rosenthal (straight solid arrow), the internal cerebral veins (curved solid arrow), the straight sinus (straight open arrow), and the superior sagittal sinus (arrowhead). The imaging plane (coronal, transverse, or sagittal) affects the visibility of the venous system at 2D TOF MR angiography but not at 3D phase-contrast MR angiography.

 

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TABLE 4. Ranking of the Six MR Angiographic Sequences by the Results of the Friedman Test
 
In Table 4, a ranking of the six sequences by the results of the Friedman test is shown. Sagittal and transverse TOF MR angiography were ranked lowest by the individual observers and by all of the observers together. Similar results were found by performing the Friedman test for separate observers. The visibilities of the separate 28 structures was different from the overall visibility.

The Cochran Q test was used to assess the performance of the six sequences for separate structures. It was used to identify some structures for which another sequence was better than the sequence that performed best according to the results of the Friedman test (Table 3). For instance, sagittal 2D TOF MR angiography enabled better visualization of the sphenoparietal sinus than did coronal 2D TOF MR angiography.

To evaluate interobserver variability in the assessment of the visibility of the intracranial venous system, a {kappa} value was calculated for each pair of observers for each sequence. For this calculation, the 12 volunteers and 28 structures were pooled. The 36 {kappa} values thus obtained ranged from 0.36 to 0.71, which indicated a moderate to good agreement between observers.


    DISCUSSION
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
At MR angiography, flow gives rise to high signal intensity, and the absence of flow is characterized by reduced signal intensity. However, reduced signal intensity can also occur in the presence of flow because of phenomena such as spin saturation and intravoxel phase dispersion (12). Spin saturation occurs whenever intravascular spins are not allowed to recover from previous radio-frequency pulses. This may be circumvented by not making the repetition time too short and by selecting an imaging plane that is perpendicular to the direction of flow. Spin saturation is also dependent on the flip angle, which should not be too large; it should be smaller for 3D MR angiography than for 2D MR angiography. Intravoxel spin phase dispersion occurs because of the wide spectrum of flow velocities within a voxel, the higher orders of motion, and the inhomogeneity of the magnetic field. The effects of this phenomenon may be limited by decreasing the voxel size, by shortening the echo times, and by using flow compensation. These general measures to limit artifactual signal loss are well established and should be applied in any MR angiographic protocol to increase the sensitivity to flow.

However, even if these general measures are taken, specific MR angiographic sequences (2D TOF, 3D TOF, 2D phase contrast, and 3D phase contrast) differ in their susceptibility to artifactual signal loss. From the literature, it is not clear how these sequences perform with respect to the visualization of the intracranial venous system. The first aim of this study was to determine the performance of these sequences.

From our pilot study, it was apparent that 3D TOF MR angiography was unsuitable for use in the visualization of the intracranial venous system because of in-plane saturation. Three-dimensional TOF MR angiography is more susceptible to spin saturation because the effects of in-plane saturation are more likely to occur in the selected volume than in the single section selected at 2D TOF MR angiography (12).

In addition, we found that 2D phase-contrast MR angiography was inappropriate for use in the visualization of intracranial venous structures because substantial intravascular signal loss occurred, presumably because of intravoxel dephasing in the large voxels used with this technique. Three-dimensional phase-contrast MR angiography was less affected by this deterioration because of the smaller voxels used. Thus, 2D TOF and 3D phase-contrast MR angiographic sequences are useful for imaging the intracranial venous system.

The orientation of the imaging plane with respect to the blood vessels should be considered when an MR angiographic protocol is designed. As mentioned before, the imaging plane should be perpendicular to the direction of flow to limit in-plane saturation (13). However, the intracranial venous system is a complex 3D structure in which blood flows in many directions. Therefore, in any imaging plane, some blood flows in-plane and thus becomes more susceptible to signal loss.

Since relevant disease may occur anywhere in the intracranial venous system, the protocol should be designed to cover the whole venous system. To maximally limit the saturation effects, such a protocol would ideally include the acquisition of images in three orientations that are perpendicular to each other. In ill patients, however, such a protocol would be too time-consuming. Therefore, the protocol should include only one MR angiographic sequence, but this sequence should provide enough information. The second aim of this study was to assess the effect of the acquisition plane on the visualization of the normal intracranial venous system at phase-contrast and TOF MR angiography.

At 2D TOF MR angiography, the orientation of the acquisition plane is critical. In this study, the sagittal and transverse 2D TOF sequences were worse than the coronal 2D TOF sequence. In the sagittal sequence, in-plane saturation caused the visibility of sagittally oriented structures, such as the superior sagittal sinus, to deteriorate (Table 3). With the transverse sequence, the visibility of transverse structures, such as the transverse sinus (Table 3), was limited because of the same phenomenon (Fig 1). However, the coronal 2D TOF sequence permitted adequate visualization of the intracranial venous system. By using this sequence, the greatest inflow of unsaturated spins seems to be affected. Saturation effects were found only in the transverse and sphenoparietal sinuses (Table 3).

Lewin and co-authors (10) observed signal loss in the posterior part of the superior sagittal sinus with coronal 2D TOF MR angiography, and they observed spin saturation in the midline veins with a sagittal sequence. To limit these saturation effects, the authors advocate the use of a 2D TOF sequence in an oblique plane. A disadvantage of the proposed protocol is the fact that the acquisition of two series of oblique images—one perpendicular to the left transverse sinus and the other perpendicular to the right transverse sinus—is required to cover the whole venous system. Our data contrast with those of Lewin et al (10) since, in our study, the coronal TOF sequences used in the posterior part of the superior sagittal sinus were not seriously affected by spin saturation. Our study findings suggest that coronal 2D TOF MR angiography sufficiently depicts the whole intracranial venous system without the need for additional images in different planes.

At 3D phase-contrast MR angiography, the choice of acquisition plane does not measurably affect the visibility of the intracranial venous system (Fig 2). The 3D phase-contrast sequence permitted good visualization of the intracranial venous system in all three orientations of the acquisition plane. This is attributable to the fact that 3D phase-contrast MR angiography involves use of the phase shift in the MR signal induced by the flow of blood in a specified direction (12). For the reconstruction of a phase-contrast image, flow-sensitive transverse, coronal, and sagittal images are combined (12). Our results showed a considerable difference between the three 3D phase-contrast MR angiographic sequences only in the veins of the septum pellucidum (Table 3). These veins were better depicted with the coronal sequence, presumably because of the perpendicular orientation of this sequence with respect to the vascular course.

In this study, we demonstrated that the normal intracranial venous system is adequately visualized at 3D phase-contrast MR angiography and at coronal 2D TOF MR angiography. In addition, we found it possible to adequately visualize the whole venous system with any of these sequences. In the overall visualization of the intracranial venous system, 3D phase-contrast and coronal 2D TOF sequences performed better than did sagittal and transverse 2D TOF sequences (Table 4). However, differences in the visibility of individual venous structures at 3D phase-contrast MR angiography and coronal 2D TOF MR angiography were found (Table 3).

Because of the complex 3D structure of the intracranial venous system, dedicated MIP images are required to limit superimposition. We generated two transverse MIP images, a caudal image that displayed the deep venous system without superimposition of the cortical veins and a rostral image that showed only the cortical veins. We also generated a midsagittal MIP image that depicted the deep venous system without superimposition of the lateral veins. In this way, structures such as the straight sinus were well depicted without superimposition of, for example, the inferior anastomotic veins. In our study, these three MIP images were sufficient for the visualization of the whole venous system.

We assessed TOF MR angiography and phase-contrast MR angiography in the normal intracranial venous system. Both have advantages and disadvantages. Acquisition times are longer for phase-contrast MR angiography than for TOF MR angiography. Therefore, the former is more susceptible to motion artifacts. However, contrary to TOF MR angiography, phase-contrast MR angiography always gives a clear distinction between flow and thrombus (methemoglobin); both of these phenomena may show high signal intensity on TOF images (14). T1-weighted spin-echo images may not always help in the differentiation between flow and thrombus, since the hyperintensity of methemoglobin might be confused with the hyperintensity of flow-related enhancement. Thus, the possibility of distinguishing between flow and thrombus with phase-contrast MR angiography might be an advantage in the detection of intracranial venous occlusive disease.

A prospective clinical trial is necessary to determine if 3D phase-contrast MR angiography (in any plane) enables better detection of intracranial venous occlusive disease than does 2D TOF MR angiography. At 3D phase-contrast MR angiography, the imaging plane (coronal, transverse, or sagittal) does not affect the visibility of the intracranial venous system. In a future study, coronal 2D TOF MR angiography and 3D phase-contrast MR angiography in any orientation would have to be compared in patients with suspected intracranial venous occlusive disease.


    Acknowledgments
 
We thank R. J. van der Geest, MS, for permitting us to use his automated method for the quantification of flow velocity.


    Footnotes
 
Abbreviations: MIP = maximum intensity projection TOF = time of flight 2D = two-dimensional 3D = three-dimensional

Author contributions: Guarantor of integrity of entire study, M.A.v.B.; study concepts, L.L., M.A.v.B., M.N.J.M.W.; study design, L.L., M.A.v.B.; definition of intellectual content, L.L., M.A.v.B., M.N.J.M.W.; literature research, L.L.; clinical studies, L.L.; data acquisition, L.L.; data analysis, L.L., M.A.v.B., F.T.d.B., R.v.d.B.; statistical analysis, J.H., A.S.; manuscript preparation, L.L., M.A.v.B.; manuscript editing, L.L., A.S.; manuscript review, M.A.v.B., J.H., M.N.J.M.W.


    References
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Curé JK, Van Tassel P, Smith MT. Normal and variant anatomy of the dural venous sinuses. Semin Ultrasound CT MR 1994; 15:499-519.[Medline]
  2. Rippe DJ, Boyko OB, Spritzer CE, et al. Demonstration of dural sinus occlusion by the use of MR angiography. AJNR Am J Neuroradiol 1990; 11:199-201.[Medline]
  3. Mattle HP, Wentz KU, Edelman RR, et al. Cerebral venography with MR. Radiology 1991; 178:453-458.[Abstract/Free Full Text]
  4. Tsuruda JS, Shimakawa A, Pelc NJ, Saloner D. Dural sinus occlusion: evaluation with phase-sensitive gradient-echo MR imaging. AJNR Am J Neuroradiol 1991; 12:481-488.[Abstract]
  5. Medlock MD, Olivero WC, Hanigan WC, Wright RM, Winek SJ. Children with cerebral venous thrombosis diagnosed with magnetic resonance imaging and magnetic resonance angiography. Neurosurgery 1991; 31:870-876.
  6. Vogl TJ, Bergman C, Villringer A, Einhaupl K, Lissner J, Felix R. Dural sinus thrombosis: value of venous MR angiography for diagnosis and follow-up. AJR Am J Radiol 1994; 162:1191-1198.[Abstract/Free Full Text]
  7. Yuh WTC, Simonson TM, Wang AM, et al. Venous sinus occlusive disease: MR findings. AJNR Am J Neuroradiol 1994; 15:309-316.[Abstract]
  8. Isensee C, Reul J, Thron A. Magnetic resonance imaging of thrombosed dural sinuses. Stroke 1994; 25:29-34.[Abstract]
  9. Dormont D, Sag K, Biondi A, Wechsler B, Marsault C. Gadolinium-enhanced MR of chronic dural sinus thrombosis. AJNR Am J Neuroradiol 1995; 16:1347-1352.[Abstract]
  10. Lewin JS, Masaryk TJ, Smith AS, Ruggieri PM, Ross JS. Time-of-flight intracranial MR venography: evaluation of the sequential oblique section technique. AJNR Am J Neuroradiol 1994; 15:1657-1664.[Abstract]
  11. van der Geest RJ, Niezen RA, Van der Wall EE, De Roos A, Reiber JHC. Automated measurements of volume flow in the ascending aorta using MR velocity maps: evaluation of inter- and intraobserver variability in healthy volunteers. J Comput Assist Tomogr 1998; 22:904-911.[Medline]
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