Magnetic resonance angiography: current status and future directions
© Hartung et al; licensee BioMed Central Ltd. 2011
Received: 25 October 2010
Accepted: 9 March 2011
Published: 9 March 2011
With recent improvement in hardware and software techniques, magnetic resonance angiography (MRA) has undergone significant changes in technique and approach. The advent of 3.0 T magnets has allowed reduction in exogenous contrast dose without compromising overall image quality. The use of novel intravascular contrast agents substantially increases the image windows and decreases contrast dose. Additionally, the lower risk and cost in non-contrast enhanced (NCE) MRA has sparked renewed interest in these methods. This article discusses the current state of both contrast-enhanced (CE) and NCE-MRA. New CE-MRA methods take advantage of dose reduction at 3.0 T, novel contrast agents, and parallel imaging methods. The risks of gadolinium-based contrast media, and the NCE-MRA methods of time-of-flight, steady-state free precession, and phase contrast are discussed.
Clinical applications for Magnetic Resonance Angiography (MRA) are rapidly expanding as technological advances in both hardware and imaging techniques overcome previous limitations, and the risks from intravenous contrast agents and repeated ionizing radiation exposure become more salient for the clinician and patient . Magnetic resonance imaging (MRI) has the advantage of relying on the intrinsic magnetic properties of body tissues and blood in an external magnetic field to produce an image, without the need of ionizing radiation or nephrotoxic contrast agents. With the increasing availability and use of 3.0-Tesla (T) magnets, which received FDA approval in 2002, and optimized pulse sequences, high-quality images with excellent spatial resolution can be obtained in shorter scan times with smaller or no injections of contrast agents. In this manuscript we will review recent developments in (1) performing MRA at 3.0T, including "low-dose" contrast-enhanced (CE) MRA, and (2) new non-CE (NCE) MRA techniques.
MRA at 3.0T
Typically, CE-MRA techniques are used more often than NCE-MRA techniques. Advantages of CE-MRA relative to other MRA techniques, such as time-of-flight (TOF) and phase-contrast (PC), include shorter acquisition times, improved anatomical coverage, and decreased susceptibility to artifacts caused by blood flow and pulsatility. To avoid combined arterial and venous enhancement, shorter acquisition times are necessary to obtain purely "arterial" phase images. This can be done using acquisitions with a parallel imaging or time-resolved techniques. At 3.0T, the gain in SNR can allow higher acceleration factors in parallel imaging to decrease scan times and improve spatial resolution even further [3–5].
While 3.0T opens many possibilities for the future of MRA, it also carries with it a new set of clinical and technological problems that need to be addressed before gaining widespread use. Pulse sequences that have been optimized for 1.5T may need to be adjusted for 3.0T applications. Additionally, the high magnetic field strength increases energy deposition in the patient and field inhomogeneity, as discussed below.
Contrast-enhanced MRA at 3.0T
CE-MRA has been established as a non-invasive alternative to conventional angiography in evaluating peripheral vascular disease [10–12] and can be an alternative to CTA for the diagnosis of acute pulmonary embolism . Lower-extremity MRA is typically associated with the highest contrast dose protocols of all MR imaging techniques, often requiring a double-dose (0.2 mmol/kg) or more of Gd-contrast to be administered . It has been shown that the amount of Gd-contrast needed at 3.0T for lower extremity MRA can be reduced up to one-third of that used at 1.5T (i.e. from 0.3 mmol/kg to 0.1 mmol/kg) . The resulting images at lower contrast doses had better arterial definition than high-dose images, presumably due to lower residual background signal from the initial contrast injection and less venous contamination .
Renal CE-MRA quality at 3.0T has also been evaluated with low-dose Gd. Attenberger et al. demonstrated equal image quality for evaluation of the renal arteries comparing 0.1 mmol/kg of gadobenate dimeglumine at 3.0T with 0.2 mmol/kg of gadobutrol at 1.5T . Kramer et al. compared low-dose (0.1 mmol/kg) gadopentetate dimeglumine at 3.0T with conventional digital subtraction angiography (DSA) for evaluation of renal artery stenosis in 29 patients, yielding good to excellent quality images with sensitivity and specificity of 94% and 96% respectively . These findings suggest that at 3.0T, the contrast dose in current practice is likely higher than needed, and can be lowered without negatively impacting spatial resolution or overall image quality.
Parallel imaging at 3.0T
Limitations and safety concerns for CE-MRA at 3.0T
The stronger magnetic field at 3.0T results in significant challenges and limitations that are yet to be fully overcome. Constructive and destructive interference due to RF field inhomogeneity and increased Specific Absorption Rate (SAR) are major concerns when imaging at 3.0T.
RF field inhomogeneity can result in areas of interference and loss of complete anatomic coverage within the image field. At 3.0T, the resonance frequency of protons in water is 128 MHz, double the value in a 1.5T system, which means that the radiofrequency wavelength is halved from 52 cm to 26 cm. This shortened wavelength can span the dimensions of the field of view for abdominal and pelvic imaging, occurring more frequently in persons with a large body habitus . As two RF waves overlap in the imaging field, constructive or destructive interference can result in areas of brightening or darkening respectively. A similar artifact can occur in persons with large amount of fluid in their abdomen (eg. ascites or pregnancy). Electrical current circulates within the fluid under the strong magnetic field and interferes with the RF field pulses resulting in interference . Advances in coil design, such as multicoil transmit body coils, can suppress eddy currents and improve RF field homogeniety at higher field strengths . In addition to improved coil design, new pulse sequences such as three-dimensional tailored RF pulses have been shown to improve homogeneity of the radiofrequency excitation.
RF pulses transfer energy to protons within the patient and ultimately generate heat as a byproduct of energy release. Heat produced within the patient can have detrimental physiologic effects and is carefully monitored within the imaging setting, with current limits of total body heating set by the FDA at 4 W/kg for the whole body over a 15 minute period [26, 27]. SAR provides an estimate for the energy deposited in the tissue by the RF pulse and increases with the square of the resonance frequency. At 3.0T, the resonance frequency is double that of a 1.5T system, and thus the SAR is increased fourfold . Modified pulse sequences, acquisition techniques, and hardware designs are being developed to aid in management of the increased SAR at higher fields. The use of parallel imaging also provides an important solution to this problem, as the multiple detector coils used to simultaneously encode a larger anatomic region serve to both decrease acquisition time and decrease the number of RF pulses needed to acquire an image.
Non Contrast-Enhanced Magnetic Resonance Angiography (NCE-MRA)
The widespread use NCE-MRA has been limited by prolonged acquisition times and motion artifacts that favor CE-MRA. However, several factors have contributed to a renewed interest in NCE-MRA methods, including improvements in MR hardware and software and concerns over the safety of gadolinium-based contrast in high-risk patient groups. The latter is particularly concerning, as patients with moderate to severe renal insufficiency and vascular or metabolic disorders are at risk for developing the debilitating and possibly life-threatening disease of nephrogenic systemic fibrosis (NSF) [6–8]. A recent meta-analysis by Agarwal et al.  identified the odds of developing NSF were 27 times greater in patients with chronic kidney disease (N = 79/1393, 5.7%) exposed to gadolinium compared to control subjects with chronic kidney disease (N = 3/2953, 0.1%) who did not receive gadolinium. This poses a significant imaging challenge as metabolic syndrome, diabetes and renal disease continue to afflict a larger percentage of the population each year . Also, situations may occur where NCE-MRA is preferred due to difficult IV access or contraindication of IV contrast material. High-resolution CE-MRA usually requires a large bore IV catheter that may be difficult to place in patients who are obese or with poor veins, and IV contrast agents are usually not given during in pregnancy due to teratogenic effects observed in animal studies.
NCE-MRA has been available since the beginning of MR imaging and is routinely used for intracranial imaging. It has also been validated for use in coronary, thoracic, renal and peripheral vascular disease . In a recent review, Provenzale et al.  found similar diagnostic quality in MRI combined with MRA compared to CTA for carotid and vertebral dissection without clear superiority of either method. TOF MRA has also been compared to computed tomography angiography (CTA) and digital subtraction angiography (DSA) in following treated cerebral aneurysms, and has high sensitivity in detecting residual flow within the aneurysm .
Time-of-flight (TOF) is the most commonly used NCE MRA technique, especially for peripheral and intracranial applications. TOF relies on the suppression of the background signal by rapid slice-selective radiofrequency excitation pulses that saturate the signal from stationary tissue, resulting in suppressed background signal [30, 46]. Because the venous signal could potentially obscure the visualization of the adjacent arteries, the venous flow is usually selectively suppressed by applying a saturation band on the venous side of the imaging slice to null the signal as it enters the slice being imaged. This same principle can be applied to the diaphragm during respiration and the heart during the cardiac cycle. In tissue planes with high flow velocity, the incoming blood will be free of the excitation pulse that saturates the background tissues resulting in strong signal intensity. Slow blood flow or stasis, retrograde filling, tortuous vessels, or vessels in the same plane as the image slice result in saturation of the blood flow in the image volume and poor vessel visualization.
ECG-gating has been successfully applied to CE-MRA techniques in the thoracic aorta, where cardiac motion can result in blurring of the vessel wall in the ascending portion of the aorta . For imaging the peripheral arteries, where blood flow depends on the phase of the cardiac cycle, systolic gating can be used to time the image acquisition during peak blood flow . Lanzman et al. recently describe the use of a promising novel ECG-gated 3D NCE-MRA technique in patients with peripheral artery disease, showing adequate image quality and disclosure of significant arterial stenoses in the lower extremities without the need for exogenous contrast media.
Steady-State Free Precession MRA
In a retrospective analysis by François et al.  of 23 patients who underwent both CE-MRA and 3D SSFP of the thoracic aorta, measurement of the aortic diameter was essentially equal between the two methods with notably superior visualization of the aortic root using 3D SSFP. A separate study compared CE-MRA to 3D SSFP for the evaluation of pulmonary veins (PV) prior to radiofrequency ablation surgery, and the 3D SSFP images demonstrated accurate PV diameter measurements with superior SNR and CNR . A study by Krishnam et al.  demonstrated that free-breathing ECG-gated SSFP MRA of the thoracic aorta had equal diagnostic sensitivity and specificity compared to CE-MRA in 50 patients with suspected thoracic aorta disease. Independent qualitative and quantitative image analysis showed both techniques providing excellent visibility grades of all aortic segments. SSFP MRA demonstrated better visibility of the aortic root and had higher SNR and CNR values for all segments, while allowing the patient to breathe freely during imaging.
3D SSFP MRA has also been applied to the evaluation of the renal arteries. Maki, et al. compared 3D SSFP MRA to CE-MRA at 1.5T in 40 patients and showed that 3D SSFP MRA had a sensitivity of 100% and specificity of 84%. Similarly, Wyttenbach, et al.  evaluated 53 patients suspected of renal artery stenosis with 3D SSFP and CE-MRA at 1.5T, with 3D SSFP MRA having a sensitivity and specificty of 100% and 84%, respectively. A study by Lanzman et al.  compared the image quality and visibility of renal arteries at 1.5T and 3.0T and demonstrated a significant gain in SNR and CNR at 3.0T of 13-16% and 16-23% respectively, with the greatest improvement of mean image quality at the segmental artery branches. The gain, while significant, is less than expected by the theoretically doubling of SNR anticipated at 3.0T due to SSFP relying on contrast from T2/T1 ratio.
ASL is limited by relying on arterial velocity to replace blood in the imaging plane with tagged blood. In peripheral arteries with slower flow, the inflow of tagged blood can approach the T1 of the surrounding tissues, thus eliminating the tagging effect. This can be partially overcome by the multiple, thinner-slab acquisitions, but at the expense of longer imaging times.
In summary, recent improvements in MRI hardware and software have lead to dramatic changes in the techniques used for MRA. The greater use of 3.0T scanners for MRA combined with improved parallel imaging methods have brought about a paradigm shift in CE-MRA toward a "less is more" approach. Further reductions in intravenous contrast administration have been made possible with the availability of novel intravascular contrast agents. The other recent major development in MRA has been the renewed use of NCE-MRA methods. Although NCE-MRA methods still require longer scan times than CE-MRA methods, they do offer several advantages over CE-MRA, including reduced risk to patients and lower costs. Interestingly, phase-contrast NCE-MRA methods offer the potential to provide additional hemodynamic information that currently is obtained using invasive methods.
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