Applied Radiology

Magnetic resonance angiography (MRA) is an established technique for the evaluation of the cerebral vasculature and is rapidly gaining acceptance as an alternative to peripheral angiography. Historically, however, MRA of the thorax has been limited by the requisite long acquisition times and multiple motion vectors resulting in severe image degradation. In recent years, advanced magnetic resonance (MR) systems that are capable of sub-second image acquisitions, the routine use of intravascular gadolinium and, in the case of coronary artery imaging, the development of "navigator echoes" have significantly improved image quality, permitting exquisite detailing of the thoracic vasculature.1-3 This article describes the basic MRA techniques and the recent technologic advancements that permit diagnostic quality thoracic MRA.

Basic MRA techniques

The basic concept of MRA is to suppress the signal emanating from stationary tissues in the body and enhance the signal from flowing blood. There are two techniques commonly used clinically: phase-contrast and time-of-flight MRA. Each of these techniques can be acquired as a series of continuous two-dimensional (2D) slices or a single three-dimensional (3D) volume. The advantages and disadvantages of each technique relative to thoracic MRA is presented below.

Phase-contrast MRA

Phase-contrast (PC) MRA utilizes two opposing flow-encoding gradients to produce a phase shift in moving protons. The phase shift describes a vector with both velocity and directional information. From the diagram in figure 1 we can see that flow information can only be evaluated in protons moving along the axis of the flow-encoding gradients. To describe flow in all directions, at least four pairs of flow-encoding gradients must be applied across the tissues.l Because of the need for additional gradients, PC-MRA is quite time consuming. In addition, this technique is exquisitely sensitive to motion, a significant disadvantage in the dynamic environment of the chest. Cardiac and respiratory gating can be utilized to reduce the associated motion artifacts from physiologic thoracic activity, but this is at the expense of additional acquisition times. Although impressive images quantitating flow through the coronary arteries have been demonstrated,4 the requisite long acquisition times limit the routine use of PC MRA in the chest.

Time-of-flight (TOF) MRA

The object of TOF-MRA is to suppress the T1 signal from background tissues and enhance the T1 signal emanating from flowing blood in each image. This task is accomplished through saturation of the stationary background spins.

Saturation-When hydrogen protons in a large magnetic field are exposed to a resonant radiofrequency, the individual protons jump to a higher energy state against the main magnetic field. The result is a gradual loss of longitudinal magnetization (figures 2A-C). When the radiofrequency is switched off, the protons gradually return to the lower energy state, the longitudinal magnetization recovers, and the excess energy is given off in the form of heat (figure 2D). This is known as T1 relaxation.

The T1 relaxation is a finite interval that differs for various compounds and tissues; it is the basis for contrast on a T1-weighted image. Some tissues recover very fast (short T1) and others take a little longer (long T1). The percent recovery just before the next radio pulse will determine the amount of T1 signal for each compound. By selecting a short repetition time (TR), we can maximize the contrast between tissues (figures 3A, B). However, if we fire a series of rapid radio pulses, one right after another, none of the tissues will have time to recover and no T1 signal will be produced.

In TOF-MRA, the T1 signal from a slice or slab of tissue is saturated with a series of rapid radio pulses (figure 3C). As such, no appreciable signal emanates from the stationary protons in that slice. However, blood flowing into this area does not experience the saturation pulses and enters the slab fully relaxed, with a maximal longitudinal magnetization. After the next radio pulse, the background tissues remain saturated while the fresh spins in the flowing blood produce a high T1 signal. This is the basis for vascular contrast in TOF-MRA.

One of the limitations with TOF-MRA is the saturation effects the blood experiences as it flows through the imaged tissue volume. This is more problematic with thicker tissue volumes and slow blood flow, areas where the blood experiences multiple saturation pulses for an extended period of time, resulting in severe signal drop-off at the distal end of the volume.

2D vs 3D acquisition

One way to limit the saturation effects of TOF MRA is to acquire a series of thin, individual slices through the anatomic area of interest and stack the individual sections to produce a volumetric image of the vasculature. This is referred to as a 2D acquisition. Because the individual slices are thin, the blood doesn't experience multiple saturation pulses as it traverses the imaged tissue slice. However, disadvantages of 2D acquisitions include inter-slice motion which results in severe post-processing image degradation, and the relative poor quality multiplanar reformations due to the finite thickness of each slice.1,2 This is especially problematic in the chest, where the intricate architecture of the thoracic vasculature may warrant the use of complex reformations to delineate the tortuous course of the coronary and pulmonary vessels.3,5

In a 2D acquisition, the thickness of each slice is limited by the strength of the gradient oriented along the slice selection axis. The steeper the gradient, the thinner the tissue section excited for a given radiofrequency (rf) pulse. In a 3D acquisition, an entire volume of tissue is initially excited with a single rf pulse. The individual slices in that volume are then determined by multiple phase encoding steps applied along the slice selection direction. Because this process is relatively independent of the gradient strength, very thin sections (<1 mm) can be acquired. This technique allows for detailed postprocessing reconstructions of the complex vascular anatomy present in the chest. The trade-off, of course, is the severe signal drop-off at the distal end of the tissue slab, resulting from the multiple saturation pulses the blood experiences as it traverses the imaged volume. However, the recent introduction of a number of new imaging techniques, combined with the latest advanced scanner hardware, has effectively eliminated the in-plane saturation effects and motion artifacts, making 3D-TOF the optimal technique for imaging the thoracic vasculature.6 The remainder of this article describes these advances and their effect on image quality.

Fast scanners

A scanner's speed is directly related to the maximum amplitude and the rise time of the gradient subsystems. The latest generation of MR units are equipped with high powered gradient coils that permit fast scanning techniques which can markedly reduce acquisition times and permit single breath-hold evaluations of the chest. At our institution, a 3D-TOF volumetric image of the thoracic vasculature can be obtained in 19 seconds. In addition, the improved frequency and phase resolution between adjacent spins afforded by the powerful gradients in conjunction with a shorter rise time permits a faster readout following a radio pulse and, thus, significantly reduces the minimum echo time (TE). The effect is an improved signal-to-noise ratio resulting from decreased intravoxel dephasing of spins (figure 4).

Intravascular gadolinium

In general, gadolinium increases the T1 signal of the vasculature by markedly decreasing the T1 relaxation time of the blood. In one study, administration of an IV dose of 0.3 mmol/kg Gd-DTPA was found to reduce the T1 relaxation of blood from 1200 ms to 300 ms.7 In other words, it doesn't take as long for the longitudinal magnetization to recover following an excitation.

With regards to our 3D-TOF acquisitions, the short repetition time of the saturation pulse suppresses the T1 signal from all the tissues in the imaged slice. However, the gadolinium in the vasculature markedly shortens T1 relaxation and allows the protons within the blood to at least partially recover their longitudinal magnetization before the next radio pulse. Thus, a higher T1 signal is maintained within the vasculature relative to the stationary background tissues despite the series of saturation pulses. In essence, vascular enhancement is no longer flow dependent.8,9

At our institution, all MRA images of the thoracic vasculature are obtained with gadolinium-DTPA contrast. A total of 0.2 mmol/kg body weight is administered intravenously at 2 cc/second. Imaging begins immediately with a series of 3 to 5, 19-second 3D-TOF breath-hold sequences and a 3-second breath between each series. Depending on the desired vascular phase, optimal contrast enhancement usually is achieved by the third or fourth series (figure 5).

Respiratory and cardiac gating

The standard 3D, contrast-enhanced MRA images of the thoracic aorta and pulmonary vasculature are acquired over multiple cardiac cycles. Therefore, the final images are actually composites of the systolic and diastolic phases of the heart. Alternatively, cardiac activity can be electronically monitored and the interval between contractions (R-R interval) subdivided into predetermined "bins." During image acquisition, the acquired data is placed in the bin that corresponds to the current position along the R-R interval. Therefore, each bin contains the image data for a single phase of the cardiac cycle. This is the definition of cardiac gating. When the images from each bin are played in a cine loop, a dynamic evaluation of heart wall motion and vascular pulsations can be appreciated. A similar technique can be used to gate respiratory activity.

Evaluation of the coronary arteries warrants special consideration. The relatively small diameter of these vessels compared to the excursion distance associated with a normal cardiac contraction requires accurate cardiac gating to "freeze" wall motion during data acquisition. Because image data can only be collected during a finite portion of the R-R interval, a 3D volume can not be completed during a single breath-hold. As such, respiratory gating must be used in conjunction with cardiac gating to accurately image the proximal coronary arteries.3,5,10,11

In the past, volumetric images of the proximal coronary arteries could be obtained by segmenting the acquisition into a series of suspended respirations.12 A mechanical device was used to measure the excursion of the chest wall and would then provide feedback to the patient through audible or visual ques. These ques would help the patient reproduce the degree of inspiration after each breath.13-16 This, of course, would require full patient cooperation. A novel technique for gating respiratory motion without the need of external mechanical devices or significant patient cooperation is the use of "navigator echoes" to monitor the superior-inferior (SI) position of the hemidiaphragm.3

Kinematic studies of heart motion during respiration have demonstrated that cardiac displacement is mainly in an SI direction. In addition, there is essentially a linear relationship between the diastolic position of the heart and the SI position of the hemidiaphragm.17 The navigator echo is simply a thin, longitudinally oriented volume that intermittently monitors the SI position of the hemidiaphragm and determines the interval of acceptable data acquisition. Thus, patient cooperation is no longer essential for effective coronary imaging (figure 6).3

Clinical applications

The advantages of thoracic MRA over standard angiographic techniques in the chest include its ability to acquire volumetric 3D images of the vessels noninvasively without ionizing radiation or iodinated intravenous contrast. A review of current and preliminary clinical applications relative to specific sections of the thoracic vasculature is provided below.

Pulmonary arteries

Pulmonary embolism-Pulmonary embolism is one of the major causes of mortality in the hospitalized patient.18 The standard diagnostic techniques, V/Q scan and angiography, are both time consuming and invasive. Recent advances in CT angiography show promise in the evaluation of central and paracentral pulmonary emboli.19-21 However, iodinated intravenous contrast materials are still necessary with this technique.

For a number of technical reasons, MRA of the pulmonary arteries historically has been extremely limited. As mentioned above, uncompensated respiratory and cardiac motion significantly degrade vascular detail. Overlapping venous and arterial vessels produce complex images which may be very difficult to interpret.6 Also, depending on the age of a thrombus, its appearance on a standard spin-echo sequence can range from low to high signal intensity.22-24 Contrast-enhanced thoracic 3D MRA has the potential to overcome at least some of these limitations.

The homogeneous intravascular signal intensity provided by the IV gadolinium allows thrombus to appear as a true filling defect, regardless of blood flow.6 Advanced high speed MR systems permit fast 3D acquisitions that are capable of high resolution imaging of the entire pulmonary vasculature within a single breath-hold (< 20 seconds) (figure 7). In the severely tachypneic patient, acquisition times can be further reduced by using 1/2 k-space sampling in the phase-encoding direction, or by reducing the number of partitions in the 3D volume, though this is at the expense of spatial resolution.6 Initial reports describe a high diagnostic accuracy in the evaluation of central pulmonary embolus utilizing these techniques.25

The overlapping arterial and venous vasculature remains a problem. However, the 3D acquisition permits reformations in additional planes to help delineate the complex anatomic architecture and localize filling defects within the arterial system.

Pulmonary arterial hypertension- MRA has been demonstrated to effectively and noninvasively diagnose pulmonary artery hypertension.6,26 With gadolinium-enhanced MRA, we have the ability to visualize the pulmonary arteries to the sub-segmental level, allowing clear demonstration of the abrupt caliber change from the central to the peripheral vasculature. In addition, recent reports have shown that thoracic MRA may be useful in distinguishing primary pulmonary hypertension from secondary hypertension due to chronic thromboembolic disease.26

Thoracic aorta

Dissection and aneurysm-Following the diagnosis of aortic dissection, evaluation of the extent of disease becomes imperative in order to determine the direction and urgency of therapeutic intervention. The efficacy of MR imaging in the assessment and follow-up of aortic dissection is well established.27,29 However, conventional MRI suffers technical limitations related to the variable blood flow present within the false lumen that may preclude differentiation of clot from sluggish flow; differentiation of thrombus from turbulent flow in large aortic aneurysms may be difficult with standard MR techniques for the same reasons.4,6 In addition, requisite long acquisition times may be problematic in the hemodynamically unstable patient. Contrast-enhanced MRA, with or without breath-hold, has been shown to overcome these limitations.6 Because vascular enhancement is no longer flow dependent with contrast-enhanced MRA techniques, differentiation of thrombus from sluggish flow is readily apparent (figure 5). The 3D acquisition permits detailed reconstructions in additional planes to accurately characterize the extent of dissection relative to branch vessels (figure 8). Finally, fast scanning techniques permit an expedient diagnostic evaluation of the hemodynamically unstable patient.

Congenital abnormalities-3D MR angiography of the pulmonary vessels can accurately characterize anatomical anomalies such as a right-sided or double aortic arch, as well as aberrant branch vessels. Contrast-enhanced MR angiography can be used in conjunction with cardiac gating to produce cinegraphic images of blood flow and provide both physiologic and anatomic information in disease entities such as aortic coarctation (figure 9) or valvular stenosis. Intravenous gadolinium enhancement eliminates the flow-related artifacts caused by turbulent conditions distal to the stenosis, thus permitting accurate localization and quantification of the degree of narrowing.6

Coronary arteries-To date, MR imaging of the coronary arteries has been very limited, mostly due to motion artifacts caused by cardiac and respiratory activity. These can be at least partially compensated for with gating techniques such as the navigator echo sequence described above.3 Because the arteries are close to the myocardial surface and often embedded in epicardial fat, magnetization transfer and fat suppression techniques have been utilized to suppress the signal from the myocardial and fatty tissues, respectively, and improve conspicuity of the proximal vessels.11 Nonetheless, accurate characterization of coronary artery disease with MRA is not currently possible. Recent reports describe the experimental use of ultrafast MR imaging with a first-pass bolus gadolinium-enhancement technique to measure and quantify myocardial perfusion in a single heart beat, thus providing indirect evidence of coronary artery disease.30 However, at the time of this writing, gadolinium-enhanced MR coronary angiography remains largely experimental.

Conclusion

High speed imaging techniques in combination with the routine use of intravenous gadolinium is currently capable of producing diagnostic quality, three-dimensional magnetic resonance angiographic images of the thoracic vasculature in a single, comfortable breath-hold. Cardiac gating can be utilized to segment image acquisitions and produce high quality cinegraphic images of cardiac activity. In short, 3D TOF-MRA with intravenous administration of gadolinium-DTPA contrast has proven efficacy in the diagnosis of thoracic vasculature pathology. With further development and improvement of intravenous contrast agents and the routine use of sub-second imaging techniques, thoracic MRA will likely see an expanded role in the diagnosis of thoracic vascular abnormalities. AR

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Dr. Klioze and Dr. Mergo are with the Department of Radiology at the University of Florida College of Medicine in Gainesville, FL.