MRA of the Pulmonary Circulation 28

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K. Nael, MD; J. P. Finn, MD

David Geffen School of Medicine, UCLA Radiol Sci, BOX 957206, 3371, VUB, Los Angeles, CA 90095-7206, USA

C O N T E N T S

28.1 Introduction 307 28.2 CE-MRA Techniques 307 28.3 Recent Advances 308

28.4 The Role of Pulmonary CE-MRA in Clinical Applications 309 28.4.1 Pulmonary Embolism 310

28.4.2 Pulmonary Arterial Hypertension 312 28.4.3 Complex Congenital Heart Disease 312 28.4.4 Tumors 313

28.4.5 Venography 314 28.5 Conclusion 315

References 317

MRA of the Pulmonary Circulation 28

Kambiz Nael and J. Paul Finn

28.1

Introduction

Computed-tomography angiography (CTA) is widely regarded as the technique of choice for non-invasive workup of acute and chronic pulmonary vascular disease. The success of CTA in the thorax is due in part to the high spatial resolution of CT, and advances in multi-slice technology have dramatically increased the speed and simplicity of CTA. However, lack of exposure to ionizing radiation and using a safe, non- nephrotoxic contrast agent, in addition to its capabil- ity of multiplanar imaging over a large ﬁ eld of view, make 3D contrast-enhanced MR angiography (CE- MRA) a compelling alternative diagnostic modality for workup of pulmonary circulation.

Over the past decade thanks to numerous advances in pulse sequences and scanner hardware and software, the image quality and reliability of 3D CE- MRA has gained wide acceptance, moving from the experimental ﬁ eld into clinical practice. This chapter describes existing state-of-the-art 3D CE-MRA techniques for the assessment of the pulmonary circulation. Developing tools that are likely to enhance the future impact of pulmonary CE-MRA are highlighted.

Finally, current clinical experience and clinical applications of CE-MRA in the pulmonary vasculature are summarized.

28.2

CE-MRA Techniques

CE-MRA relies on the T1-shortening effect of paramagnetic contrast agents in the vascular bed during the image acquisition (Prince et al. 1993) and is typically performed using a T1-weighted fast spoiled 3D gradient-recalled-echo (GRE) pulse sequence.

Recent advances in hardware and software technology have played an important role in the evolution of CE-MRA in terms of temporal and spatial resolution.

With the newest generation of MR gradients, including a slew rate of up to 200 mT/m/ms and gradient strengths up to 45 mT/m, a 3D GRE sequence with TR of about 2 ms and TE of about 1 ms is now achievable, allowing the acquisition of an entire high-resolution 3D data set in less than 20 s breath-hold. Reﬁ nements such as asymmetrical echo and different k-space sampling schemes have also improved the performance of CE-MRA.

Controlled contrast administration is an essential component of CE-MRA. To ensure image quality, it is well recognized that the low-spatial-frequency k-space data, which are principally responsible for image contrast, should be aligned with the peak vascular enhancement during a gadolinium-enhanced

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308 K. Nael and J. P. Finn

3D MRA (Earls et al. 1996; Kreitner et al. 2001).

Reliable timing can be achieved by use of a test bolus scan prior to the administration of the full contrast- media volume. Alternatively, some workers use real- time bolus monitoring, with or without centric k- space reordering (Foo et al. 1997; Ho and Foo 1998).

Both approaches can be used successfully, and the choice of which to use depends on user preference and, to some extent, vendor platform.

Besides the conventional way of performing CE- MRA, integration of ultrafast MR techniques can now generate temporally resolved 3D MRA, which depict the transit of the paramagnetic contrast agent through the vascular system (Finn et al. 2002;

Korosec et al. 1996). This allows a real-time visuali- zation of the ﬁ rst pass of a contrast bolus that pre- viously has been a unique feature of conventional X-ray angiography.

Ultra-short TR sequences, in combination with sparse k-space sampling, can result in acquisition of 3D data sets in time frames ranging from a few seconds to a fraction of a second (Finn et al. 2002).

Higher frame rates can be achieved by reducing the size of k-space, which is regularly updated. Speciﬁ c examples using this approach include “keyhole”

imaging (van Vaals et al. 1993) and other “data sharing” techniques such as time-resolved imaging of contrast kinetics (TRICKS) (Korosec et al.

1996), or time-resolved echo-shared angiographic technique (TREAT) (Fink et al. 2005); cf. Chaps. 7 and 11. The advantage to these approaches is that the major contribution to image contrast lies in the data, which are updated frequently, and interpolat- ing the high-spatial-frequency data yields full 3D k-space datasets, i.e., high spatial resolution. A general limitation of time-resolved MRA techniques is that the spatial resolution of the individual 3D data set is limited when compared to single-phase MRA acquisitions and, with data sharing, only the low-spatial-frequency data have the prescribed temporal resolution. This latter limitation can be addressed by applying parallel-imaging techniques, using arrays of surface coils and receiver channels to reduce the number of phase-encoding steps to be measured (De Zwart et al. 2004; King et al. 2001; Bodurka et al. 2004; Hayes and Roemer 1990), improving both temporal and spatial resolution (Fink et al. 2003). It seems likely that imaging at higher magnetic ﬁ elds, such as 3 T, may be helpful in overcoming the signal-to-noise-ratio (SNR) limitations accompanying fast imaging techniques (Nael et al. 2006a).

28.3

Recent Advances

Parallel imaging (Sodickson et al. 2000; Weiger et al. 2000; Pruessmann et al. 1999; Griswold et al.

2002) represents one of the most signifi cant recent advances in MR imaging and offers improved performance over a range of MRA applications. Tra- ditionally, spatial encoding with MRI has been accomplished by the use of imaging gradients and spatially selective RF pulses. With parallel imaging, component coil signals in an RF coil array are used to partially encode spatial information by substitut- ing for phase-encoding gradient steps that have been omitted. Therefore, only a fraction of k-space, defi ned by the acceleration factor, is sampled, and then the whole dataset is reconstructed afterward. In theory, the acquisition can be accelerated by a factor equal to the number of coil elements in the array (Sodickson et al. 1997). However, in practice SNR represents a fundamental challenge and is increasingly limiting as acceleration advances. As the acceleration factor increases, the noise is also amplifi ed. Independently, decreased acquisition time leads to deterioration of image SNR.

The major strategies to counteract the SNR deterioration of parallel-imaging techniques are employ- ing higher magnetic ﬁ elds, minimizing noise ampli- ﬁ cation through improvement and adjustment in array coil geometry and sensitivity, or use of a contrast agent with greater T1 relaxation (Weiger et al.

2001; de Zwart et al. 2002). To offset acquisition- and reconstruction-related SNR losses associated with parallel imaging, practical parallel imaging should include the use of many-element arrays and an MR system with a large number of receiver channels.

The suitability of the coil array geometry for certain protocol parameters such as slab dimension and ori- entation can be quantiﬁ ed by the so-called g-factor (Pruessmann et al. 1999) (cf. Chap. 3), and gener- ally improves with the number of coil elements used.

Coils with an improved (closer to 1) g-factor allow parallel imaging with higher acceleration rates while minimizing noise amplifi cation. As a result, appropri- ately designed array coils with better sensitivity pro- fi les and more channels will improve the overall SNR, the effi ciency of parallel imaging and result in higher spatial resolution (De Zwart et al. 2004; King et al.

2001; Hayes and Roemer 1990).

Today, surface-coil arrays with up to 32 channels and MR systems with up to 32 independent wide-

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band receiver channels have become available commercially (Hardy et al. 2004; Zhu et al. 2004). The introduction of multi-element RF receiver coils and the associated multi-channel RF receiver electron- ics, combined with more effective implementation of parallel imaging, has introduced “multi-channel parallel data acquisition” as the latest addition to the fast-imaging toolbox. Increasing the number of receiver channels and/or phased-array coil elements can potentially improve the SNR and provide larger ﬁ elds of view, with good temporal and spatial resolution (Fig. 28.1). This offers the promise of highly accelerated imaging.

Three-Tesla whole-body MR systems are also now commercially available. The promise of higher SNR in comparison to 1.5 T (Willinek et al. 2003;

Campeau et al. 2001) can be used to reduce acquisition time, improve spatial resolution, or a combination of both (Campeau et al. 2001; Robitaille et al.

2000; Thulborn 1999). Implementation of fast-imaging tools such as time-resolved MRA sequences and parallel acquisition at 3.0 T provides new options for more efﬁ cient use of fast image acquisition (Fig. 28.2).

Also, since the longitudinal relaxation time, T1, of unenhanced blood increases with ﬁ eld strength, sensitivity to injected gadolinium agents for CE-MRA is

heightened, adding the advantage of using less contrast material. The SNR advantage at 3 T is especially noticeable for MRA applications.

There is growing evidence that high-magnetic- ﬁ eld CE-MRA may substantially enhance the performance of CE-MRA in clinical applications. At our institution, we use CE-MRA at 3 T for evaluation of multiple vascular territories, including the pulmonary (Nael et al. 2005a; Nael et al. 2005b; Nael et al. 2006), the carotid (Nael et al. 2006a), abdominal (Michaely et al. 2005) and lower extremity (Nael et al. 2006a) circulations. Based on very satisfactory results, we have incorporated 3-T CE-MRA into our routine clinical practice.

28.4

The Role of Pulmonary CE-MRA in Clinical Applications

As CTA continues to be widely regarded as the technique of choice for the workup of acute and chronic pulmonary vascular disease, there will remain a subset of patients who, due to renal impairment,

Fig. 28.1a–c. Coronal a and sagittal-oblique b thin MIP and coronal-oblique full-thickness MIPs c from a high-spatial-resolu- tion CE-MRA in a subject with severe pulmonary stenosis, show post-stenotic dilatation of the left pulmonary artery. The data was acquired on a 32-channel 1.5-T MR scanner, using 26 phased-array coil elements. By integration of parallel acquisition (GRAPPA algorithm, acceleration factor R=2), the entire 3D data set was acquired in a 19-s breath-hold with voxel dimension of 1×1×1 mm³, over a 500-mm ﬁ eld of view

c b

a

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contrast-media sensitivity, or radiation burden, are not good candidates for CTA. There is, therefore, a role for magnetic resonance angiography (MRA) in the lungs. MR imaging of the pulmonary vasculature has been challenging for a variety of reasons, including respiratory motion and susceptibility artefacts at air-tissue interfaces.

With current hardware, MRA can now resolve up to ﬁ fth-order pulmonary branches in a single short breath hold (Nael et al. 2005a). Time-resolved MRA is helpful for lung imaging and can reveal the dynamic information in vascular beds with rapid circulation such as the pulmonary vasculature (Finn et al. 2002;

Goyen et al. 2001; Hatabu et al. 1999; Nicolaou et al.

2004). Time-resolved MRA can provide insight into cardiopulmonary hemodynamics (Figs. 28.3 and 28.4). Enhancement of lung parenchyma and ﬁ lling patterns in arterivenous ﬁ stulae, shunts, and congenital heart anomalies may be best appreciated by highly temporally resolved imaging.

28.4.1

Pulmonary Embolism

There are several studies that have described the use of pulmonary MRA for pulmonary embolism (PE) with high sensitivity and speciﬁ city in large lobar and segmental vessels (Meaney et al. 1997; Steiner et al.

1997; van Beek et al. 2003; Gupta et al. 1999). The sensitivity decreased for emboli in the subsegmental vessels (Gupta et al. 1999; Meaney et al. 1999).

Dynamic MRA may provide supplemental functional and perfusion information, which can help in the diagnosis of pulmonary embolism (Fink et al. 2004;

Kluge et al. 2004) (Fig. 28.5a,b).

Currently, the role of MRA in PE is mostly for follow-up of stable patients and chronic pulmonary embolism. Another advantage of MRA over alternative diagnostic strategies for work-up of patients with suspected PE relates to the fact that it can be comple- mented by MR venography of the pelvic and femoral

Fig. 28.2a–c. Coronal MIP series from time-resolved MRA a shows sequential ﬁ lling of the pulmonary and systemic vasculatures.

By using a four-segmented echo-shared sequence and aggressive parallel acquisition (GRAPPA, R=4) at 3.0 T a high-temporal (1 s) and high-spatial-resolution (1×1.2×3 mm³) 3D time-resolved MRA was obtained. Coronal volume-rendered b and full- thickness MIPs c from high-spatial-resolution CE-MRA show the pulmonary arterial tree with extreme details up to the ﬁ fth order branches. By implementing aggressive parallel acquisition (GRAPPA, R=4) and use of a 32-channel body array coil at 3 T, the entire 3D data set was acquired during an 18-s breath-hold and with voxel dimension of 0.7×0.7×0.8 mm³

b a

c

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Fig. 28.3a,b. Coronal MIPs from time-resolved MRA a (GRAPPA, R=2, temporal resolution 1.5 s) and coronal MIP image from high-spatial-resolution CE-MRA b (voxel dimension of 1×1×1.5 mm³ over a 500-mm ﬁ eld of view in a 19-s breath- hold, using GRAPPA with an acceleration factor of R=2 at 1.5 T) show stenotic and hypoplastic left pulmonary artery. In the perfusion phase of the time-resolved MRA, note the delayed enhancement of left parenchyma and decreased perfusion, indicating the signiﬁ cance of the left pulmonary artery stenosis

Fig. 28.4. Evaluation of the signal intensity versus time from a time-resolved MRA shows early enhancement of the aorta (yellow line) before the peak enhancement of the pulmonary artery (red line). This indicates the presence of a right-to-left shunt and Eisenmenger pathophysiology in this subject with severe pulmonary hypertension and right-sided heart failure

a

b

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veins (Fig. 28.5c). The signs of chronic pulmonary embolism on MRA include vascular webs and bands, wall thickening, distal arterial tapering and multiple distal perfusion defects (Ley et al. 2003).

Although pulmonary MRA may still not be practical in acutely ill patients with severe shortness of breath, its role is likely to increase as advanced techniques make their way into routine clinical practice.

28.4.2

Pulmonary Arterial Hypertension

Pulmonary arterial hypertension (PAH) is diagnosed when pulmonary arterial pressure is greater than 30 mmHg by cardiac catheterization and can be either primary or secondary to congenital heart disease, chronic lung disease, or chronic thromboembolism.

CE-MRA is a very useful non-invasive test to identify PAH, where a decrease in the number of

segmental or subsegmental pulmonary arteries and abnormal tapering of segmental vessels (pruning) are characteristic ﬁ ndings (Ley et al. 2003; Laffon et al. 2001; Kreitner et al. 2004; Nikolaou et al. 2005) (Fig. 28.6). Time-resolved MRA permits direct visual- ization of shunts and concomitant velocity-encoded cine MRI and phase-contrast MRA can provide valu- able information regarding cardiac function and chamber size, as well as quantitative measurements of blood velocity and ﬂ ow in the pulmonary arteries (Hoeper et al. 2001; Saba et al. 2002); cf. Chap. 43.

28.4.3

Complex Congenital Heart Disease

Since most congenital heart abnormalities tend to present early in life, CE-MRA is gaining interest as a non-invasive diagnostic measure for both primary diagnosis and follow-up imaging. Congenital-heart-

Fig. 28.5a–c. Coronal MIP images a and coronal thin-MIP from the arterial phase b of a time-resolved MRA show the sequen- tial ﬁ lling of pulmonary arteries and parenchymal enhancement. Several regions of ﬁ lling defects in right and left pulmonary arteries (arrows) indicate the presence of extensive thrombo-embolism. The decreased parenchymal enhancement in the right upper and lower lobe indicates the perfusion defect as a result of pulmonary embolism. The 3D data sets were acquired with in-plane resolution of 1.5×1.2 mm² and temporal resolution of 1.5 s, using GRAPPA with an acceleration factor of R=2 at 1.5 T.

Axial T1-weighted fat-saturated image of the thighs c shows presence of extensive thrombosis in the right femoral vein

c a

b

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disease patients are patients for life and require con- tinuous follow-up into adult life. In many ways, MRI is the clear front runner for evaluation of patients with congenital heart disease. Complex cardiac and vascular anatomy can be depicted by cine MRI and 3D CE-MRA, and the ability to rotate the 3D data is a very useful feature (Fig. 28.7). Congenital vascular shunts can be intracardiac, such as atrial or ventricular septal defects, or extra-cardiac, such as patent ductus arteriosus, aorto-pulmonary window or intra-pulmonary shunt. Time-resolved MRA can be extremely useful in detecting shunts and in char- acterizing their ﬂ ow direction. The postoperative follow-up of congenital heart disease is a powerful

and exciting application for pulmonary CE-MRA (Fig. 28.8); cf. Chap. 31.

Cardiac cine and velocity-encoded cine imaging can provide additional diagnostic information about cardiac function, ﬂ ow and velocity quantiﬁ cation across the cardiac valves and shunt fraction in a single non-invasive examination session.

28.4.4 Tumors

Pulmonary CE-MRA may play an important role as a part of pre-surgical evaluation for mediastinal or

Fig. 28.6a–c. Coronal a, sagittal b and axial c thin-MIP (20 mm) im- age a of CE-MRA at 3 T shows signiﬁ cant dilatation of central pulmonary arteries and abnormal proximal-to-distal tapering (pruning) of the pulmonary arteries in a subject with pulmonary arterial hypertension. The 3D data set was acquired during an 18-s breath- hold with a voxel dimension of 0.7×0.9×1 mm³, using GRAPPA with an acceleration factor of R=3

at 3 T c

b a

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lung tumors (Kauczor et al. 1992). Acquisition of the second or thrid run should be performed as a major complication of thoracic tumors is the obstruction of thoracic central veins due to the compressive effect or secondary inﬁ ltration. The combination of CE-MRA and a T1-weighted pre- and post-contrast imaging for assessment of the tumor in coronal and axial planes is extremely useful in visualizing tumor exten- sion, involvement of the vasculature and evaluation of surrounding soft tissue, and can be used for pre- surgical planning.

Fig. 28.7a–c Coronal a, sagittal b and axial c thin-MIP images from a high-spatial-resolution CE-MRA in a 21-year-old subject with repair of tetralogy of Fallot, reveal- ing a pulmonary-artery conduit with valve (a, arrow), coursing from the right ventricular outﬂ ow tract to the main pulmonary trunk. The conduit shows narrowing after the valve toward the left main pulmonary artery (c, arrow). (voxel dimen- sion of 1×1×1.5 mm³, over a 500-mm ﬁ eld of view in 19-s breath-hold, using GRAPPA with R=2 at 1.5 T)

28.4.5 Venography

Typically, there are two superior and two inferior pulmonary veins. Altered development of the pulmonary venous system typically results from persistent com- munication with the systemic system, manifesting as anomalous pulmonary venous drainage (Fig. 28.9a).

These abnormalities can be either complete or partial and are often associated with intracardiac congenital heart diseases such as a sinus-venosus-type atrial

c a b

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septal defect (Fig. 28.9b). Several studies have shown the feasibility and accuracy of 3D CE-MRA in the depiction of anomalous pulmonary venous return and the location of drainage (Prasad et al. 2004).

Pulmonary venous mapping is another indication for pulmonary venography. In patients with atrial fi brillation, RF ablation has emerged as a treatment of choice in many patients with curative potential. CE-MRA has been shown as a powerful tool for pulmonary venous mapping in preparation for catheter-guided RF ablation therapy of ectopic arrhythmogenic foci in these patients (Fig. 28.10). CE-MRA can be used as an accu- rate diagnostic tool to defi ne pulmonary venous anatomy, improve pre-procedural planning and decrease fl uoroscopic procedural time as well as post-procedural follow-up (Tsao and Chen 2002; Collins et al. 2002).

28.5 Conclusion

In the appropriate patient population, all relevant disease entities of the pulmonary vasculature can be evaluated using 3D CE-MRA, sometimes more comprehensively than with any other single modality. The addition of time-resolved MRA is appropriate for assessing high-flow vascular lesions, shunts and congenital heart anomalies. Parallel imaging and multi-element coil technology can further improve the performance of 3D CE-MRA in order to achieve higher temporal and spatial resolution and the role of 3-T imaging remains to be fully defined.

Fig. 28.8a,b. Coronal MIP from a time-resolved MRA a (in-plane resolution 1.6×1.3 mm², temporal resolution 1.2 s, GRAPPA, R=2) and coronal full-thickness MIP from high-spatial-resolution CE-MRA b (1×1×1.5 mm³ voxels, over a 500-mm ﬁ eld of view in 20-s breath-hold, using GRAPPA with R=2 at 1.5 T) in a 21-year-old subject with single ventricle and transposition of great arteries (TGA), repaired with Fontan operation. Fontan shunt is widely patent, providing the pulmonary artery ﬂ ow and perfusing both lungs symmetrically. There is no evidence of right-to-left or left-to-right shunting. The proximal part of the left subclavian artery is occluded, as a result of a previous Blalock-Tausig shunt

a

b

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Fig. 28.9a,b. Coronal volume-rendered image a from a high-spatial-resolution CE-MRA (voxel dimension of 1×1×1 mm³, over a 450-mm ﬁ eld of view in 18-s breath-hold, using GRAPPA with R=2 at 1.5 T) showing partial anomalous pulmonary venous return with a prominent left vertical vein (arrow), draining into the left brachiocephalic vein. Four-chamber-view cardiac SSFP cine MRI b shows the presence of sinus-venosus-type ASD, as a common association with this anomaly

Fig. 28.10. 3D volume-rendered image from a CE-MRA defi nes pulmonary venous anatomy, which can improve pre-procedural planning and decrease fl uoroscopic procedural time during the ablation treatment of ectopic arrhythmogenic foci in patients with atrial fi bril- lation. By implementing fast parallel imaging (GRAPPA, R=3) at 3 T, the entire 3D data set was acquired during an 18-s breath-hold with voxel dimension of 0.8×0.8×1 mm³

b a

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