Applications of Time-Resolved MR Angiography

Abstract

OBJECTIVE.

The purpose of this essay is to describe the basic principles behind contrast-enhanced time-resolved MR angiography (MRA) performed with the time-resolved imaging with stochastic trajectories technique and to show examples of the versatile applications of this technique in the evaluation of pathologic conditions throughout the body.

CONCLUSION.

Time-resolved MR angiography is a versatile technique for vascular imaging throughout the body. It can be used to answer a variety of clinical questions; to acquire diagnostically useful information, even about complicated vascular lesions; and to overcome many of the limitations of bolus-chase contrast-enhanced MR angiography. The technique is particularly useful when the arterial arrival time is uncertain, the patient is freely breathing, or contrast dynamics are critical to a diagnosis.

Spatial resolution and temporal resolution are competing objectives in MRI, including MR angiography (MRA) [1, 2]. High spatial resolution is needed to visualize small vessels, and high temporal resolution is desirable for moving beyond anatomy and visualizing dynamic processes. Traditional contrast-enhanced bolus-chase MRA has noteworthy limitations, particularly in multiple phase acquisition, due to the reduced temporal resolution afforded by long acquisition times [3]. Moreover, bolus-chase MRA requires synchronization between bolus arrival, image acquisition, and, if needed, breath-holds. This process can be difficult and even impossible, as when a patient has altered hemodynamics or cannot perform breath-holds (e.g., is freely breathing or is a sedated child or infant) and when images obtained in multiple phases are necessary. Advances in hardware, parallel imaging, and sequence design have allowed the implementation of techniques that enable fluoroscopic visualization of vascular anatomy [4–6]. This essay illustrates the versatility of time-resolved MRA and the range of anatomic locations and clinical questions to which it can be applied.

Technique

All studies were performed with a 3-T system (Magnetom Verio, Siemens Healthcare) with time-resolved imaging with stochastic trajectories, which is a gradient-echo 3D view-sharing time-resolved MRA technique [7, 8]. The k-space is fully sampled in the center (termed region A) and undersampled at the periphery (region B) with a quasirandom sampling scheme. Factors most affecting imaging speed—the sizes of regions A and B, degree of undersampling of B, and parallel imaging acceleration—were tailored to the case, allowing a flexible approach to the clinical question, the desired anatomic coverage, and temporal versus spatial resolution.

Three-dimensional volumes were obtained at 2- to 5-second intervals for several minutes after injection of a gadolinium chelate. A timing test bolus was not needed, preventing preprocedure contamination of the vasculature. The imaging parameters varied depending on the dimensions of the region of interest and the flow characteristics of the pathologic condition being studied. The parallel imaging acceleration factor ranged from 2 to 6, the size of the A region from 14% to 20% of the k-space, and the percentage of region B sampled with each pass through the center from 40% to 50%. TR/TE was minimized, temporal resolution ranged from 1.8 to 4.7 s/frame, and the voxel sizes were 0.8 × 0.9 × 0.9 to 1.1 × 1.4 × 1.5 mm. The temporal footprint of each frame depended on the temporal resolution per frame and the number of frames that contributed data to each frame (fraction sampling of B region per pass). Gadobenate dimeglumine (MultiHance, Bracco) was used for all adults, and gadopentetate dimeglumine (Magnevist, Bayer HealthCare) was used for pediatric patients. Dosing was 0.05 mmol/kg for distal lower extremity runoff and for evaluations that required more than one contrast dose, such as that of a patient with Raynaud disease. In all other cases, the dose was 0.1 mmol/kg.

Applications

Head and Neck

Evaluation of an arteriovenous malformation (AVM) in the brain is an important application of time-resolved imaging with stochastic trajectories [9]. Time-resolved MRA facilitates localization of the arterial supply and determination of the size and location of the AVM nidus and the number and type of draining veins, which can be used to determine the surgical grade of the lesion. Initial inflow images depict all four arteries that supply the brain (Fig. 1). A key component in the diagnosis of an AVM, particularly when small, is an early draining vein, which is visualized with dynamic imaging. In addition, structural MRI can be performed in the same session, which enables exact localization of the AVM and assessment of the eloquence of the adjacent neural structures.

Fig. 1 —

41-year-old man with right temporal lobe arteriovenous malformation (AVM) discovered after intracranial hemorrhage.

A, Axial T2-weighted MR image shows cluster of flow voids representing AVM nidus (arrow) in right temporal lobe.

B, Early arterial phase time-resolved imaging with stochastic trajectories MR angiographic image shows opacification of both internal carotid arteries and vertebral arteries. Right temporal AVM is supplied by right middle cerebral artery (open arrow) and posterior cerebral artery (solid arrow).

C, Late arterial phase time-resolved imaging with stochastic trajectories MR angiographic image shows early draining vein to vein of Galen (arrow), a deep venous structure that affects prognosis and therapeutic options.

Thorax

Time-resolved MRA is particularly important in thoracic imaging because it obviates long breath-holds. This feature is particularly important when breath-holds are not possible, as in imaging of nonintubated sedated patients undergoing monitored anesthesia care. The technique allows robust venous mapping of the central veins of the chest and facilitates detection of stenosis and vascular anomalies and evaluation of the collateral flow to further define hemodynamic significance and chronicity [10, 11] (Fig. 2). The dynamic and fluoroscopic capability of time-resolved imaging with stochastic trajectories affords three-phase evaluation of the pulmonary vasculature, which owing to isotropic resolution can be viewed in any plane. In addition, concomitant angiographic and perfusion data sets can be obtained, and qualitative and relative or semiquantitative evaluation of lung perfusion becomes possible.

Fig. 2 —

52-year-old man with left superior pulmonary vein occlusion after radiofrequency ablation for atrial fibrillation.

A, Coronal oblique CT angiographic image shows atresia of upper lobe arteries (arrow), likely due to decreased upper lobe perfusion and stasis. Arrowhead indicates left superior pulmonary vein occlusion.

B, Coronal time-resolved imaging with stochastic trajectories arterial phase MR angiographic (MRA) image shows correlation of absence of arterial inflow to left upper lobe (arrow).

C, Coronal time-resolved imaging with stochastic trajectories venous phase MRA image shows lack of venous opacification in left upper lobe (arrow) and occlusion of left superior pulmonary vein (arrowhead).

Contemporaneous MRA and perfusion images have been found helpful in the diagnosis of chronic thromboembolic pulmonary hypertension because the occluded artery and affected pulmonary parenchyma can be evaluated concurrently [12] (Fig. 3). The dynamic imaging capabilities of time-resolved MRA even at a low dose of gadolinium contrast material are illustrated in Figure S4, which shows thoracic outlet syndrome in a 10-year-old girl who had a 50-mm decrease in systolic blood pressure with the arm elevated. (Figures S4–S10, cine loops, can be seen in the AJR electronic supplement to this article, available at www.ajronline.org.) The examination was performed in two phases: with the affected arm in neutral position, revealing no remarkable findings, and with the arm elevated, resulting in external impression on the right subclavian artery and delayed arterial flow to the arm. Bolus arrival times were not needed for this child, who was unable to cooperate because of anxiety.

Fig. 3 —

59-year-old woman with long-standing progressive dyspnea, enlarged right ventricle, and mosaic pattern to lung parenchyma on chest CT scans consistent with pulmonary hypertension. Perfusion MRI showed that hypertension was due to chronic thromboembolic disease.

A, Coronal time-resolved imaging with stochastic trajectories MR angiographic image shows contrast material in right ventricle and pulmonary arteries. Arrow shows lack of opacification of left lower lobe pulmonary artery.

B, Anteroposterior conventional angiogram of chest confirms lack of arterial flow to left lung base.

C, Posterior ventilation-perfusion scan shows lack of perfusion to left lower lobe.

Abdomen and Pelvis

Time-resolved imaging with stochastic trajectories yields dynamic information on the abdominal and pelvic blood vessels (both native and transplanted), expanding on the anatomic information obtainable with bolus-chase MRA (Figs. 5 and 6). As in the chest, time-resolved MRA eliminates the need for long breath-holds and is particularly useful in evaluating pediatric, elderly, and nonintubated sedated patients. The decision to emphasize spatial or temporal resolution can be determined by the clinical demands of a study—for example, in the evaluation of renal artery stenosis, the need for spatial resolution prevails [13], but in other situations, such as evaluation of arteriovenous fistula, dynamic information and temporal resolution are more important. Not only the secondary collateralization but also the precise location of the arteriovenous fistula can be visualized in the frame in which arteriovenous communication is seen (Fig. 7). Another application is evaluation of pelvic congestion syndrome, in which reflux into the gonadal veins can be readily visualized with a single gadolinium bolus [14].

Fig. 5 —

13-year-old boy who has undergone renal transplant. Time-resolved MR angiography shows anatomic detail of dual arterial supply not seen with ultrasound, at which finding was “increased velocity in main renal artery.” See also Figure S5E, cine loop, in supplemental data online.

A–C, Arterial (A), parenchymal (B), and venous (C) phase time-resolved imaging with stochastic trajectories MR angiographic images obtained for evaluation of renal artery stenosis show dual arterial supply from common aortic patch, which was grafted end to side to common iliac artery (open arrow, A). Renal vein is anastomosed to external iliac vein (arrowhead, C). White arrow (A) indicates external iliac artery.

D, Posterior volume-rendered image shows arterial anastomosis in more detail (upper arrow) than A–C. Solid arrow indicates internal iliac artery; open arrow, external iliac artery. No renal artery stenosis is present.

Fig. 6 —

3-year-old free-breathing patient with right diaphragmatic hernia and surgically proven ectopic right kidney. Because of unusual anatomy and young age of patient, examination would be impossible with bolus-chase MR angiography. See also Figure S6C, cine loop, in supplemental data online.

A, Contrast-enhanced MR image shows ectopic right kidney superior to liver.

B, Coronal arterial phase time-resolved imaging with stochastic trajectories MR angiographic image shows right kidney adjacent to right atrium (solid arrow) with hypoplastic right renal artery originating from aorta at level of celiac axis. Aneurysm of right renal artery (open arrow) also is evident. Kidney was found at surgery to be malrotated with hilum facing laterally.

Fig. 7 —

34-year-old man with history of deep venous thrombosis after motor vehicle accident. Because of massive thigh swelling, thrombectomy was attempted. Femoral vein to femoral vein bypass ultimately was performed and was complicated by iatrogenic arteriovenous fistula (unknown at time of surgery). Bolus-chase MR angiography was attempted a few days before this study, but the images were difficult to interpret owing to extensive venous enhancement. Fistula was suspected, but communication was identified only with time-resolved MR angiography. See also Figure S7C, cine loop, in supplemental data online.

A, Coronal arterial phase image of thigh allows anatomic localization of fistulous connection between femoral artery and vein (open arrow) and femoral vein bypass graft (solid arrow).

B, Coronal venous phase image illuminates extensive tortuous venous collateralization.

Extremities

There can be extreme variability in contrast arrival times between patients and even between the extremities in one patient. This variability can be due to altered cardiac status, proximal stenosis, or an underlying pathologic condition that affects one limb only and makes bolus-chase MRA difficult. Furthermore, venous contamination occurs in a small but not insignificant number of examinations, also owing to altered cardiac status or a pathologic condition in one limb, such as cellulitis [3]. Time-resolved imaging with stochastic trajectories overcomes these limitations by enabling routine fluoroscopic visualization of the lower extremities (often with a half dose or less of contrast material), and therefore disparate arrival times cease to matter. A clinical scenario solved with time-resolved MRA without invasive conventional angiography is popliteal entrapment syndrome, an uncommon but potentially incapacitating condition among young athletes (Fig. 8). We have also routinely used time-resolved MRA for preoperative anatomic evaluation of the presence and configuration of the fibular artery and normal anterior and posterior flow into the foot before harvesting fibular bone grafts for reconstructive surgery. This technique is a lower-contrast-dose alternative to bolus-chase MRA and prevents venous contamination [15, 16] (Fig. 9). Congenital and posttraumatic vascular malformations of the upper and lower extremities can be evaluated noninvasively with time-resolved imaging with stochastic trajectories to discern the diagnosis and to evaluate vascular anatomy for surgical planning (Figs. 10 and 11). Conditions requiring provocative testing also can be evaluated. For example, Raynaud disease can be evaluated at multiple temperatures [17] (Fig. 12).

Fig. 8 —

34-year-old marathon runner with claudication on minimal exertion. Examination was performed in plantar flexion, which can be used as provocative maneuver if initial findings are normal. Popliteal entrapment syndrome is secondary to anomalous muscular or tendinous anatomy that compresses popliteal artery, potentially leading to arterial thrombosis, aneurysm, and thromboembolic complications. See also Figures S8D and S8E, cine loops, in supplemental data online.

A, Coronal arterial phase time-resolved imaging with stochastic trajectories MR angiographic image shows arterial collateralization and occlusion of popliteal artery (arrow) representative of advanced popliteal entrapment. Delayed arterial flow to affected foot can be determined by comparison with contralateral foot.

B, Axial T2-weighted MR image of knee shows anomalous insertion of medial head of gastrocnemius muscle coursing between compressed popliteal artery (white arrow) and popliteal vein (black arrow). Standard anatomic imaging is essential part of MRI evaluation because vascular findings can be subtle.

C, 25-year-old patient with normal knee. Axial T2-weighed MR image of knee shows normal position of popliteal artery (white arrow) and vein (black arrow) in popliteal fossa.

Fig. 9 —

In preoperative consideration for fibular graft, it is ideal to identify normal three-vessel arterial distribution in leg so that fibular artery can be removed with graft and arterial supply to foot is not compromised.

A, 50-year-old patient undergoing time-resolved imaging with stochastic trajectories MR angiography for evaluation of fibular flap for bone reconstruction. Coronal arterial phase oblique image of right leg shows fibular arterial supply to posterior aspect of foot (solid arrow) and diminutive right posterior tibial artery (open arrow).

B, Coronal arterial phase oblique image of left leg in same patient shows only two-vessel supply to foot. Both of these congenital variations are rare, but are contraindications for fibular flap harvest.

C, 33-year-old man with normal arterial supply. Time-resolved MR angiographic image shows anterior tibial artery supplying dorsal aspect of foot (solid arrow), fibular artery terminating just above ankle (open arrow), and posterior tibial artery supplying plantar aspect of foot (arrowhead).

D, 57-year-old woman with buccal carcinoma. For mandibular reconstruction, head and neck surgeon prefers to harvest fibula contralateral to mandibular resection to allow proper cosmetic angulation. Time-resolved MR angiographic image shows desired right leg anatomy is not conducive to fibular graft because fibular artery supplies dorsal aspect of foot (arrowhead), and anterior tibial artery terminates early (arrow).

Fig. 10 —

57-year-old woman with swelling and discoloration in finger. Vascular steal from unaffected digits is evident. See also Figure S10D, cine loop, in supplemental data online.

A, Early arterial phase time-resolved MR angiographic image shows predominance of arterial flow to arteriovenous malformation in fourth digit.

B, T2-weighted sagittal MR image of fourth digit shows abnormal flow voids in dorsal aspect (arrow).

C, Late arterial phase time-resolved MR angiographic image.

Fig. 11 —

8-year-old boy with deep lacerations of right leg due to fall into fish tank and persistent difficulty walking after initial healing. Surgeon visualized anterior tibial artery pseudoaneurysm on ultrasound images but requested time-resolved MR angiography because of palpable thrill over same artery. Time-resolved imaging with stochastic trajectories MR angiographic image shows adjacent arteriovenous fistula that necessitated change in management from ultrasound-guided thrombin injection to endovascular coiling of both arteriovenous fistula and pseudoaneurysm (large arrow). Small arrows indicate early draining vein overlying anterior tibial artery.

Fig. 12 —

39-year-old patient with Raynaud disease. Both images are from same temporal frame obtained with two separate injections. One-half dose (0.05 mmol/kg) was used for each injection, enabling evaluation in same setting. Other suspected conditions for which provocative maneuver testing has been successfully performed (not shown) are popliteal artery entrapment syndrome, subclavian steal syndrome, and median arcuate ligament syndrome.

A, Time-resolved MR angiographic image obtained after initial contrast injection with hands in warmer shows multisegmental high-grade stenosis of digital arteries, which has attenuated appearance even after warming, reflecting chronic disease.

B, Time-resolved MR angiographic image obtained after second contrast injection after exposure to ambient cool air shows lack of opacification of superficial arches (particularly left) and near-complete lack of enhancement of digital arteries.

Conclusion

The images and conditions discussed in this essay emphasize the versatility of time-resolved MRA in answering clinical questions throughout the body, particularly in conditions where bolus-chase MRA is too slow to provide relevant temporal information. Time-resolved MRA can provide critical time course data to characterize pathology, can eliminate venous contamination, and can be used with patients in whom bolus-chase MRA would fail due to motion and acquisition constraints.