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(Radiology. 1999;211:865-869.)
© RSNA, 1999

Technical Developments

Pulmonary MR Angiography with Ultrasmall Superparamagnetic Iron Oxide Particles as a Blood Pool Agent and a Navigator Echo for Respiratory Gating: Pilot Study1

K. Håkan Ahlström, MD, PhD, Lars O. Johansson, Johanne B. Rodenburg, PhD, A. Sgrimur Ragnarsson, MD, Per Åkeson and Arve Börseth, MSc

1 From the Department of Radiology, Uppsala University, Sjukhusvagen 5-11 Akademiska Sjukhuset, 751 85 Uppsala, Sweden (K.H.A., L.O.J.); Philips Medical Systems, Best, the Netherlands (J.B.R.); the Department of Radiology, Örebro Medical Center Hospital, Örebro, Sweden (A.S.R.); and Nycomed Amersham Imaging, Oslo, Norway (P.A., A.B.). Received April 7, 1998; revision requested June 29; revision received September 8; accepted December 9. Supported in part by a grant from Nycomed Amersham Imaging. Address reprint requests to K.H.A.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
In nine healthy adult volunteers, pulmonary magnetic resonance angiography was performed with the blood pool agent NC100150 Injection combined with respiratory gating with a navigator echo. With increasing doses of the contrast agent, higher signal intensities and vessel branch order visualization were achieved. No motion artifacts were seen. The blood pool agent NC100150 Injection in combination with respiratory navigator gating permitted acquisition of high-quality MR angiograms of the pulmonary vasculature during continuous breathing.

Index terms: Embolism, pulmonary, 60.72 • Iron • Lung, MR, 60.121412, 60.12142, 60.12143 • Magnetic resonance (MR), contrast enhancement, 60.121412, 60.12142, 60.12143 • Magnetic resonance (MR), maximum intensity projection, 60.12149 • Magnetic resonance (MR), technology, 60.121412, 60.12142, 60.12143 • Magnetic resonance (MR), vascular studies, 60.121412, 60.12142, 60.12143


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Magnetic resonance (MR) angiography with gadolinium-based extracellular fluid agents has gained increasing clinical application, but the short intravascular half-life of the contrast agents and the rapid redistribution into the extracellular space might be disadvantages. Blood pool agents, which have delayed clearance from the intravascular compartment, have been developed to overcome these limitations.

One type of blood pool agent is composed of ultrasmall superparamagnetic iron oxide (USPIO) particles, which were originally developed as T2 contrast agents for imaging of the reticuloendothelial system (1–3). These agents have also been found to decrease T1 and have been used for MR angiography (4–6).

Compared with extracellular fluid agents, blood pool agents provide additional possibilities for longer and repeated imaging, since imaging is not restricted to the first pass. Longer imaging times will improve the spatial resolution, which is especially important if MR angiography of the lungs with this technique is to compete with conventional pulmonary x-ray angiography.

Some difficulties are encountered at pulmonary MR angiography (eg, movements from breathing and heart beats) that make it a special challenge. Use of breath-hold techniques for gadolinium-enhanced pulmonary MR angiography has been found to result in acquisition of high-spatial-resolution images (7,8), although it is impossible to eliminate breathing artifacts in some patients (9). A technique for respiratory triggering and gating has been described previously (10) in which the patient breathes freely and a navigator echo pulse is applied for each cardiac cycle; data are accepted only if the diaphragm position falls within a narrow (3–7-mm) window around end expiration.

NC100150 Injection (Nycomed Amersham Imaging, Oslo, Norway), a colloidal preparation of USPIO particles with an oxidized starch coating, is a new blood pool agent for potential use in MR imaging and MR angiography. The aim of this study was to assess the use of a combination of the blood pool agent and navigator echoes for respiratory gating in pulmonary MR angiography.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This study was part of a clinical phase 1, open-label, single-ascending-dose investigation in healthy volunteers. The trial protocol was approved by the ethics committee of Uppsala University. All volunteers gave informed consent prior to inclusion in the study. Nine male subjects (age range, 21–26 years; mean age, 23.6 years) were divided randomly into three equal groups. Each group received three different doses—1.0, 2.5, or 4.0 mg of iron per kilogram of body weight—of NC100150 Injection (30 mg of iron per milliliter). The blood pool agent was injected into an antecubital vein as a bolus at a rate of 1–3 mL/sec. The injection was given manually through a tube and was immediately followed by a flush with 20 mL of 0.9% sodium chloride. The choice of doses was based on results in previous animal experiments (11), and the doses were administered in ascending order starting with 1.0 mg Fe/kg. The active component in NC100150 Injection consists of USPIO particles with an oxidized starch coating. The half-life of the contrast medium in pigs is approximately 150 minutes (12).

MR Angiographic Technique
The images were acquired approximately 30 minutes after injection of the contrast medium with a 1.5-T MR system (ACS-NT; Philips Medical Systems, Best, the Netherlands) with a 10 mT/m gradient system (0.6-msec rise time). The time delay was a result of other tests (including blood sampling and a perfusion study of the myocardium) performed during and immediately after the injection. A quadrature body coil was used for imaging, and a workstation (EasyVision; Philips Medical Systems) was used for postprocessing of images.

The MR angiographic protocol included a three-dimensional radio-frequency–spoiled gradient-echo sequence (repetition time of 10.0 msec, echo time of 3.1 msec, 60° flip angle, 512 x 256 matrix, bandwidth of 168 Hz per pixel, field of view of 450 mm). The echo was sampled partially with a truncation factor of 62.5% and segmented k-space sampling. Thirty-two overlapping 4.0-mm-thick sections in the coronal plane, with a left-to-right phase-encoded direction, were reconstructed to 64 2.0-mm-thick sections. Navigator echo pulses were applied with a 7-mm gating window positioned on the right diaphragm, which allowed continuous breathing. Cardiac triggering with a trigger delay of 500 msec was used. Data were acquired only during diastole. The imaging times varied between 5 and 10 minutes.

To present the data, original coronal sections, full maximum intensity projection images, sequential maximum intensity projection images (15-mm-thick volumes with 5-mm overlap), and closest vessel projection images were used.

Efficacy Evaluation
First, the signal intensities were measured in each arterial vessel branch (large enough for reliable values) on the original images. Noise was measured by calculating the SD of the signal intensity in regions of interest outside the body. The result of these measurements was presented as the signal-to-noise ratio. The diameter of each arterial vessel branch and the number of arterial branches seen in the pulmonary bed were also noted. The investigator subjectively evaluated the quality of delineation of each vessel branch by using a four-grade scale: 1, very unsatisfactory; 2, unsatisfactory; 3, satisfactory; and 4, very satisfactory (Table 1).


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  		TABLE 1. Assessment of Each Arterial Branch with Different Doses of the Blood Pool Agent
 
Second, the overall image quality was assessed subjectively with a four-grade scale: very unsatisfactory, unsatisfactory, satisfactory, or very satisfactory. Artifacts, if present, were classified as either a focal decrease or increase in signal intensity or as motion artifacts (ie, blurring of vessel borders). The effect of artifacts on the image quality was graded subjectively as follows: no effect, image quality not seriously affected, image quality seriously affected, or images not diagnostic (Table 2).


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  		TABLE 2. Subjective Assessment of Image Quality with Different Doses of the Blood Pool Agent
 
These evaluations were made by two reviewers (L.O.J., A.S.R.) who reached consensus opinion and who were not blinded to sequence parameters or doses.

Safety Evaluation
During the study procedures and for as long as 14 days after administration of the contrast medium, the subjects were observed and vital signs and electrocardiographic and physical examinations were performed to monitor for any kind of adverse event. Clinical laboratory tests included serum chemistry, hematology, urinalysis, and fecal occult blood examination.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
With increasing doses of NC100150 Injection, higher signal intensities and vessel branch order visualization were achieved and vessel delineation improved (Table 1). With the highest dose of 4.0 mg Fe/kg, the seventh branch order of the arterial vessel tree was seen in all cases, but the signal intensity was measurable in only the fourth branch order because the other vessels were too small (Fig 1, Table 1).



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  		Figure 1a. Maximum intensity projection images of pulmonary MR angiograms obtained in one patient, with 4.0 mg Fe/kg NC100150 Injection. A = arterial branches, H = head, R = right, V = veins. (a) Partial image shows mainly arterial branches. Artifacts are seen as focal signal intensity decreases and increases along each vessel. Arrow = azygos arch, IVC = inferior vena cava. Overall image quality was judged very satisfactory. (b) Image shows almost the whole investigated volume. (c) Closest vessel view shows the whole investigated volume.

 


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  		Figure 1b. Maximum intensity projection images of pulmonary MR angiograms obtained in one patient, with 4.0 mg Fe/kg NC100150 Injection. A = arterial branches, H = head, R = right, V = veins. (a) Partial image shows mainly arterial branches. Artifacts are seen as focal signal intensity decreases and increases along each vessel. Arrow = azygos arch, IVC = inferior vena cava. Overall image quality was judged very satisfactory. (b) Image shows almost the whole investigated volume. (c) Closest vessel view shows the whole investigated volume.

 


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  		Figure 1c. Maximum intensity projection images of pulmonary MR angiograms obtained in one patient, with 4.0 mg Fe/kg NC100150 Injection. A = arterial branches, H = head, R = right, V = veins. (a) Partial image shows mainly arterial branches. Artifacts are seen as focal signal intensity decreases and increases along each vessel. Arrow = azygos arch, IVC = inferior vena cava. Overall image quality was judged very satisfactory. (b) Image shows almost the whole investigated volume. (c) Closest vessel view shows the whole investigated volume.

 
The overall image quality for all images was rated as both unsatisfactory and satisfactory with the dose of 2.5 mg Fe/kg (Fig 2) and very unsatisfactory with 1 mg Fe/kg (Fig 3). Satisfactory and very satisfactory evaluations were produced with the 4 mg/kg dose (Table 2). No artifacts were seen with 1 mg Fe/kg (Fig 3). Most artifacts, both focal signal intensity increases and decreases (Fig 1), were seen with 4.0 mg Fe/kg, but these artifacts did not affect the image quality seriously (Table 2). No motion artifacts were seen with any dose.



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  		Figure 2. Maximum intensity projection image of a pulmonary MR angiogram obtained with 2.5 mg Fe/kg NC100150 Injection. Overall image quality was judged unsatisfactory. The dotted line is an artifact from the patient monitoring equipment.

 


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  		Figure 3. Partial maximum intensity projection image of a pulmonary MR angiogram obtained with 1.0 mg Fe/kg NC100150 Injection. Overall image quality was judged very unsatisfactory. The dotted line is an artifact from the patient monitoring equipment.

 
There were no serious adverse events or noticeable trends in any safety parameter. The only adverse event occurred in one subject, moderate rhinitis 7 days after the contrast agent injection that was judged not to be related to the drug. In the clinical laboratory results, total iron increased as expected, because the laboratory test method for total iron also measures the iron in the contrast agent, and the activated partial thromboplastin time increased in 50% of the subjects. No trends were seen for any other laboratory parameter. These changes were asymptomatic, transient, and possibly related to assay interference.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Pulmonary x-ray angiography, the present standard of reference for pulmonary embolism, is hampered by a minor adverse event frequency. Spiral computed tomography (CT) has been increasingly employed as a routine method in preference to pulmonary x-ray angiography. Unlike MR angiography, both these techniques use iodinated contrast media, which can be nephrotoxic, and irradiation. MR angiography with a blood pool agent has the same potential for diagnosis of pulmonary embolism as has been described for gadolinium-enhanced MR angiography with breath-hold sequences (7–9). We believe that by adding respiratory navigator gating, considerable advantages might be obtained in patients with respiratory impairment.

Compared with gadolinium-enhanced MR angiography, MR angiography with blood pool agents has the advantage of repeatability during periods of several hours without the need for additional injections of contrast agent. This quality facilitates investigations of several vascular territories (eg, the inferior vena cava, the veins of the pelvis and both legs) in one session to look for the source of pulmonary emboli.

Navigator respiratory gating functioned adequately after administration of NC100150 Injection, although the navigator signal could potentially have been disturbed as a result of several side effects from the contrast agent. Impaired navigator function could be caused by line broadening in the resonance frequency of the two-dimensional radio-frequency–selective excitation pulse. Positioning of the navigator window on the diaphragm could be problematic because signal transition is too low (ie, NC100150 Injection decreases the signal intensity of the liver to a value almost equal to that of the lungs). Also, the high signal intensity of all the enhanced lung vessels could cause the navigator correlation algorithm to fail as a result of wrong edge detection. None of these side effects were seen in our study.

It is unclear, however, whether the navigator echoes can work in patients who are referred for pulmonary MR angiography. Pleural effusion may cause difficulty in navigator gating by increasing the signal intensity of the lungs. Taylor et al (13) found that temporal changes in respiration can influence navigator echo–gated coronary MR angiography, although this may depend on the implementation of the navigator algorithm. Patients with pulmonary emboli, in particular, have irregular breathing patterns that may make proper functioning of the navigator echoes difficult. These patients may also find it difficult to remain still during a 10-minute imaging time.

The artifacts observed as a focal increase or decrease in signal intensity are thought to be due to susceptibility effects. These types of artifacts have also been described on gadolinium-enhanced MR angiograms, where they are considered to be related to the use of imaging techniques with incomplete sampling of k space (14). In our study, these artifacts might have been diminished if we had used full-echo instead of partial-echo acquisition, but that would lead to increased echo time, which would result in decreased signal intensity due to T2* decay.

To further increase signal intensity and improve image quality, a dose higher than 4.0 Fe mg/kg might be used. Then, however, use of an echo time shorter than that used in this study might be necessary to decrease the T2* effect, which otherwise would affect signal intensity when the dose is increased. Also, to diminish susceptibility artifacts, which were seen more frequently with higher doses, a shorter echo time is needed. This can be achieved with an MR imager that is more modern and has a stronger and faster gradient system than ours.

One disadvantage of blood pool agents is the simultaneous enhancement of veins and arteries, which is a problem in other vascular areas (12). Because of the short circulation time in the pulmonary circulation, some degree of venous enhancement is unavoidable; it has been reported at gadolinium-enhanced MR angiography of the lungs (8) and at spiral CT. The problem of venous overlap seen on standard maximum intensity projection images can be reduced by analyzing source images, creating multiplanar reformations, and interactively viewing the data at a workstation.

Spatial resolution with blood pool–enhanced MR angiography may improve compared to that with gadolinium-enhanced MR angiography, but it will not be as good as that with pulmonary x-ray angiography. Spatial resolution with blood pool agent–enhanced MR angiography might be improved if the field of view and the section thickness were decreased. Performance of sagittal instead of coronal imaging might be advantageous, since a rectangular field of view could be used, which would reduce the imaging time (7). Wielopolski et al (7) reported visualization of fifth vessel branch orders, and Steiner et al (8) found that 81% of the subsegmental arteries were visualized with gadolinium-enhanced MR angiography. They concluded, however, that respiratory motion and not poor spatial resolution was the major obstacle to visualization.

MR angiography with NC100150 Injection in combination with respiratory navigator gating permits high-spatial-resolution imaging of the pulmonary vasculature without breath holding. Because gadolinium-enhanced MR angiography requires first-pass imaging, free breathing is not possible when gadolinium agents are combined with the navigator echo technique. Thus, the combination of respiratory navigator gating and blood pool agents seems especially suited for pulmonary MR angiography. In the present study, we found that this combination worked well in healthy volunteers. To further evaluate this technique, it is necessary to investigate findings in patients with pulmonary embolism.


   Footnotes
 
Abbreviation: USPIO = ultrasmall superparamagnetic iron oxide

Author contributions: Guarantors of integrity of entire study, K.H.A., A.B.; study concepts, K.H.A., L.O.J., A.B., P.A.; study design, K.H.A., L.O.J., A.B.; definition of intellectual content, K.H.A., L.O.J.; literature research, K.H.A.; experimental studies, L.O.J., J.B.R., A.S.R.; data acquisition, K.H.A., L.O.J., J.B.R., A.S.R.; data analysis, K.H.A., L.O.J., A.S.R., P.A.; statistical analysis, A.B.; manuscript preparation and editing, K.H.A., P.A.; manuscript review, K.H.A., L.O.J., J.B.R., A.S.R., P.A.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Mergo PJ, Helmberger T, Nicolas AI, Ros PR. Ring enhancement in ultrasmall superparamagnetic iron oxide MR imaging: a potential new sign for characterization of liver lesions. AJR 1996; 166:379-384.[Abstract/Free Full Text]
  2. Harisinghani MG, Saini S, Weissleder R, et al. Differentiation of liver hemangiomas from metastases and hepatocellular carcinoma at MR imaging enhanced with blood-pool contrast agent Code-7227. Radiology 1997; 202:687-691.[Abstract/Free Full Text]
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  4. Anzai Y, Prince MR, Chenevert TL, et al. MR angiography with an ultrasmall superparamagnetic iron oxide blood pool agent. JMRI 1997; 7:209-214.
  5. Mayo-Smith W, Saini S, Slater G, Kaufman J, Sharma P, Hahn P. MR contrast for vascular enhancement: value of superparamagnetic iron oxide. AJR 1996; 166:73-77.[Abstract/Free Full Text]
  6. Stillman A, Wilke N, Li D, Haacke M, McLachlan S. Ultrasmall superparamagnetic iron oxide to enhance MRA of the renal and coronary arteries: studies in human patients. J Comput Assist Tomogr 1996; 20:51-55.[Medline]
  7. Wielopolski P, Oudkerk M, Hicks S, Berghout A. Breath-hold 3D MR pulmonary angiography after contrast material administration in patients with pulmonary embolism: correlation with conventional pulmonary angiography (abstr). Radiology 1996; 201(P):202.
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