Journal of Neuro-Ophthalmology, June 2009, Volume 29, Issue 2

Dynamic MRA with four-dimensional time-resolved angiography using keyhole at 3 tesla in head and neck vascular lesions.

ORIGINAL CONTRIBUTION Dynamic MRA With Four-Dimensional Time-Resolved Angiography Using Keyhole at 3 Tesla in Head and Neck Vascular Lesions Hemant Parmar, MD, Marko K. Ivancevic, PhD, Nancy Dudek, BS, Dheeraj Gandhi, MD, and Suresh K. Mukherji, MD Abstract: Conventional MRA provides inadequate visualization of the dynamic features of blood flow in vascular lesions of the head and neck. Four-dimensional time-resolved angiography using key-hole (4D-TRAK) is a new technique of performing contrast-enhanced MRA. By combining parallel imaging with sensitivity encoding (SENSE) with the keyhole imaging technique and a high field strength (3 T) magnet, we have been able to obtain detailed hemodynamic information similar to that obtained via catheter angiography with digital sub-traction (DSA), but without the risks associated with ionizing radiation exposure, iodizing contrast agents, or catheterization itself. (J Neuro-Ophthalmol 2009;29:119-127) Catheter angiography with digital subtraction (DSA) is the standard technique for imaging of the craniocer-vical vessels. With this technique, it is possible to obtain very high temporal resolution with three-dimensional (3D) reformats of multiple rotational datasets. However, because of the risks of arterial catheterization, the risks of ionizing radiation, and the costs of such procedures, safer angio-graphic procedures are being developed. MRA has gained wide clinical acceptance in evaluation of the arterial and venous anatomy of the head, neck, and spine. The two- and three-dimensional flow-sensitive MRA sequences used traditionally, such as time- Department of Radiology (HP, ND, SKM), University of Michigan Health System, Ann Arbor, Michigan; Philips Medical Systems (MKI), Cleveland, Ohio; and Department of Radiology (DGI), Johns Hopkins Hospital, Baltimore, Maryland. This paper was presented at the 45th Annual American Society of Neuroradiology (ASNR) Meeting, June 2007, Chicago, IL. Address correspondence to Hemant Parmar, MD, Department of Radiology, University of Michigan, 1500 East Medical Center Drive, Ann Arbor, MI 48109-0302; E-mail: [e-mail] of-flight (TOF) (1,2), are limited by flow-related artifacts, low spatial resolution (compared with DSA), and lack of temporal resolution (3). They are gradually being sup-planted by gadolinium contrast-enhanced magnetic reso-nance angiography (CE-MRA), particularly in visualization of high flow intracranial arteriovenous malformations (AVMs) and arteriovenous fistulas (AVFs). CE-MRA produces high-resolution 3D volume acquisitions, but the exact timing is critical for obtaining optimal image quality and accurate vasculature depiction. Centric elliptic k-space ordering has been traditionally used to acquire the peak of arterial contrast and to avoid edge enhancement artifacts (1). Contrast-enhanced timing-robust angiography (CENTRA) was subsequently intro-duced, wherein the first 4 seconds part of the central k-space is sampled randomly to sample a larger window of the arterial phase (4). Routine 3D contrast-enhanced sequences reduce some of the flow-related artifacts of TOF MRA but do not provide temporal resolution in complex lesions (5). The scan duration of a complete MRA acquisition is too long to run dynamic MRA. Limitations of a single time point acquisition include lack of dynamic information and occasionally a mistimed bolus with resultant suboptimal vessel signal or venous contamination. To image dynamic contrast kinetics, techniques based on undersampling of k-space profiles, such as temporal interpolation of k-space views (6) and keyhole (7), were initially proposed. Recently, four-dimensional time-resolved angiography using keyhole (4D-TRAK) has been introduced by combining CENTRA with parallel imaging with sensitivity encoding (SENSE) (8,9), half scan, and the keyhole technique (Fig. 1). With 4D-TRAK it became possible to accelerate dynamic MRA scans up to 60 times to a subsecond temporal sampling rate and follow contrast hemodynamics with the near-isotropic spatial resolution of 1-1.5 mm. Furthermore, a 3-T field strength magnet provides a higher signal/noise ratio that can be used to obtain images with higher spatial resolution. These J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 119 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 Parmar et al FIG. 1. Schematic representation of four-dimensional time-resolved angiography using keyhole acquisition (4D-TRAK) and reconstruction. The last dynamic is fully sampled and the peripheral part of the k-space is used to reconstruct the contrast-enhanced timing-robust angiography (CENTRA) keyhole dynamics. A precontrast fully sampled mask can be used for post-processing subtractions. improvements have allowed dynamic 3D MRA to reach a performance closer to that of DSA than achieved with other MRA techniques. We review our experience with 4D-TRAK at 3 T in evaluation of vascular abnormalities in the head and neck. METHODS Contrast-enhanced dynamic MRA with 4D-TRAK was performed on a 16-channel 3.0-T Achieva system (Philips Medical Systems, Best, The Netherlands) equipped with a commercially available eight-channel SENSE-capable head coil. Patients were positioned with a 20-gauge intravenous catheter inserted into the antecubital vein. An automated power injector (Spectris Solaris; Medrad, Warrendale, PA) was used in a biphasic injection protocol. Gadobenate dimeglumine (Multihance, 20 mL; Bracco Diagnostics Inc., Milan, Italy) was injected initially at a flow rate of 2 mL/s followed by a saline flush of 25 mL at a flow rate of 2 mL/s. The 4D MRA sequence was started immediately after the contrast injection (injection and scanning simultaneously). 4D-TRAK images were acquired using the keyhole method (7,10), partial Fourier, and CENTRA (11). In CENTRA, a central k-space cylinder is randomly filled, allowing for k-space sampling during the whole passage of the contrast bolus over time. The periphery of k-space was collected in the reference dataset at the end of the acquisition in an elliptical order, and the resulting data were used for reconstruction of each of the dynamic phases as described in the keyhole approach (Fig. 1). In addition to the CENTRA keyhole method, SENSE was implemented. The SENSE technique was used with a reduction factor of 3-3.2 in the phase-encoding direction and a reduction factor of 1.8 in the slice-encoding direction, yielding a total acceleration factor (AF) of 3 1.8. Furthermore, partial Fourier imaging was added, skipping 25% of k-space, and accelerating the k-space sampling by a factor of 1.33. Combining the techniques of 4D-TRAK yielded a total acceleration of approximately 33.75. That is, if a conventional 3D MRA required 33.75 seconds at the specified spatial resolution, it can be acquired dynamically every 1 second by this technique. Each of the individual FIG. 2. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) MRA in a normal study. Selected maximal intensity projection images in the coronal view show excellent demonstration of early arterial, late arterial, and venous phases. 120 © 2009 Lippincott Williams & Wilkins Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Dynamic MRA J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 FIG. 3. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) magnetic resonance venography (MRV) in a normal study. A. Sagittal maximal intensity projection (MIP) of acquired image series. B. Sagittal MIP after subtraction of early arterial phase preferentially displays venous kinetics. FIG. 4. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of an intracranial arteriovenous malformation (AVM). Coronal (A) and sagittal (B) maximal intensity projection images show a large AVM nidus in the left frontal lobe (arrowheads) with feeders from multiple frontal branches of the left anterior and middle cerebral arteries. Venous drainage is through a severely dilated left frontoparietal vein draining into the superior sagittal sinus and a large draining vein (arrows) emptying into the superior sagittal sinus. Deep drainage into the internal cerebral veins and vein of Galen is especially well seen on the sagittal images (arrows). 121 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 Parmar et al acceleration parameters can be adjusted to achieve up to AF = 60 on our system. Image processing included mask subtraction to sup-press the background signal of the stationary tissue. For this purpose, we used one of three dynamic volumes acquired before administration of the contrast agent with the same time-resolved MRA sequence. Depending on the field of view, resolution, and coverage adjustments on individual patients, the temporal resolution range was 1.6-3 seconds in the brain and 1.9-4.8 seconds in the carotid arteries. The in-plane acquired resolution range was 0.6-1 mm. RESULTS Dynamic MRA and magnetic resonance venography (MRV) of the head and neck using 4D-TRAK allowed the visualization of arterial, intermediate, and venous phases of vessel enhancement (Figs. 2 and 3). Anatomical detail and temporal information were obtained. Representative exam-ples are illustrated in Figures 2 through 11. Intracranial AVMs and AVFs With dynamic MRA with 4D-TRAK at 3 T, it was possible to correctly identify the normal vasculature, enlarged arterial pedicles, lesion nidus, and venous drainage pattern of an AVM and to resolve arterial and venous structures separately (Fig 4). In an AVF (Fig. 5), medium- and large-sized arterial pedicles were readily visualized, and synchronous opacification of the diseased sinus or vein indicated the arteriovenous shunt. Sometimes in AVF the direct arterial feeders or the fistula was too small FIG. 5. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of an intracranial arteriovenous fistula (AVF). Coronal maximal intensity projection images of dynamic MRA show a large tangle of vessels in the region of the left superior orbital fissure. The arterial feeders include branches from the left internal maxillary artery, left superficial temporal artery, and left ophthalmic artery (arrows). There are large venous varices within the left cavernous sinus, and some drainage is via the left superficial middle cerebral veins (arrowheads). There was no discrete nidus seen, suggesting that this is a fistula rather than a vascular malformation. 122 © 2009 Lippincott Williams & Wilkins Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Dynamic MRA J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 to visualize, but visualization of early filling of the corre-sponding vein or dural sinus would point to this abnor-mality. A more focused and thorough evaluation of these vessels could then be performed with DSA. Dural Venous Sinus Thrombosis Although 4D-TRAK provided imaging similar to that of single-phase contrast-enhanced MRV, we found that it yielded added information about venous flow patterns, collateral circulation, and intracranial circulation times, which allowed for better evaluation of this condition (Fig. 6) (12). Orbital and Neck Vascular Malformations As with intracranial AVMs, dynamic MRA with 4D-TRAK was helpful in correctly identifying normal vasculature, enlarged arterial pedicles (Fig. 7), the lesion nidus, and the venous drainage pattern in orbital AVMs (Fig. 8). MRI had the added advantage of visualization of the surrounding soft tissues. We also found this technique useful in post-treatment studies of head and neck AVMs (Fig. 7C). Carotid Body Tumor In highly vascular tumors such as carotid body tumors (paragangliomas), visualization of early arterial phase-contrast FIG. 6. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of an intracranial venous thrombosis. Coronal maximal intensity projection images show abrupt occlusion of the left sigmoid sinus with nonopacification of the left internal jugular vein (arrowheads), suggestive of venous thrombosis. Note the normal opacification of the right transverse sinus, sigmoid sinus, and internal jugular vein (arrows). 123 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 Parmar et al FIG. 7. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of an orbital arteriovenous malformation (AVM). Sagittal (A) and coronal (B) maximal intensity projection images show a large AVM (arrowheads) in the right orbital region fed by the branches of the right external carotid artery and left ophthalmic artery (arrows). A large draining vein extends over the supraorbital ridge and empties into the angular facial vein (large arrows). A three-dimensional time of flight magnetic resonance angiogram (C) shows the enlarged arterial feeders from the external carotid artery and the ophthalmic artery (arrows), but it does not provide details of the venous drainage. 124 © 2009 Lippincott Williams & Wilkins Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Dynamic MRA J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 FIG. 8. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of an orbital venolymphatic malformation. A. Postcontrast T1 coronal MRI shows a mass (arrowheads) with a small intracranial component (arrows). B. Sagittal MIP images show it as a large vascular malformation (arrowheads) with a small apical varix (arrows). enhancement within the tumor was helpful in making a correct diagnosis, as other tumors of the carotid space (such as lymphoma and nerve sheath tumor) do not show this early enhancement (Fig. 9). Such information is also helpful in guiding the surgeon during preoperative embolization. Carotid Artery Stenosis/Fibromuscular Dysplasia Using an extended field of view, the arch of the aorta and cervical and cerebral vessels could be demonstrated simultaneously in a single image. In patients with advanced atherosclerosis (Fig. 10) or fibro-muscular dysplasia (Fig. 11), delayed filling of the cerebral vessels was sometimes observed on the side of the stenotic or occluded carotid vessel (13,14). It was possible to demonstrate the patency of the distal vasculature and assess the compensatory collateral circulation. Although the information obtained from this study is analogous to that obtained by catheter angiography, the degree of stenosis was difficult to estimate accurately, and FIG. 9. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of a carotid body tumor. A. Postcontrast T1 axial fat-suppressed MRI shows an avidly enhancing mass in the right carotid space (arrowheads) that displaces vessels (arrows). B. Coronal maximal intensity projection images show early and rapid contrast enhancement of the mass, suggestive of a carotid body tumor, a diagnosis confirmed at surgery. 125 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 Parmar et al FIG. 10. Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of a carotid artery stenosis. Coronal maximal intensity projection images show severe stenosis of the proximal segments of both internal carotid arteries (arrows). other techniques such as single phase-contrast enhanced MRA or CT angiography had to be coupled with dynamic MRA. DISCUSSION We have shown cases in which 4D-TRAK imaging provided more complete hemodynamic information of the arterial and venous system in head and neck lesions than could be seen with conventional MRA. Arterial and venous phases could be separated either by simple subtraction, as used here (Fig. 3), or by more sophisticated post-processing methods based on correlation (15) or contrast arrival time (CAT) maps (16). Because 4D-TRAK forces a loss of high spatial resolution to achieve high temporal resolution, 3-T field strength is essential. To identify the more subtle features such as flow-related aneurysms or intranidal fistulas, dynamic MRA must be performed in combination with single-phase MRA, as suggested by Nael et al (17), or one must use catheter angiography. Dynamic MRA with 4D-TRAK covers the full 3D volume with adequate spatial and temporal resolution without the risks of ionizing radiation exposure, iodizing contrast agents, or catheterization itself. The 4D-TRAK technique can be applied to arterial bypass procedures to image the shunt without the risk of arterial damage from direct catheterization and to subclavian steal syndrome to demonstrate the delayed opacification of the vertebral artery (13). Although promising, this technique is not without its limitations. It requires a dedicated team consisting of a neuroradiologist, magnetic resonance physicist, and magnetic resonance technologist to adjust scanning parameters. The most significant drawback of this approach is that one must prospectively decide to favor either spatial or temporal features at the expense of the other. The current technique has relatively low spatial resolution, a problem especially in the evaluation of small AVFs, in which small fistulous portions may not be readily apparent. Improved software and higher field strength magnets will probably mitigate this problem in the future. 126 © 2009 Lippincott Williams & Wilkins Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Dynamic MRA J Neuro-Ophthalmol, Vol. 29, No. 2, 2009 FIG. 1 1 . Four-dimensional time-resolved angiography using keyhole (4D-TRAK) of fibromuscular dysplasia. Coronal maximal intensity projection images show multiple areas of vascular narrowing and dilatation, giving rise to a ‘‘beaded'' appearance (arrows) of the internal carotid and vertebral arteries. REFERENCES 1. Lanzer P, Gross GM, Keller FS, et al. 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