AJRCCM Articles in Press. Published on November 21, 2002 as doi:10.1164/rccm.200208-899OC

Pulmonary Embolism: Comparison of Angiography with Spiral CT, MRA and Real-Time MR imaging

Patrick Haage MD 1, Werner Piroth MD 1, Gabriele Krombach MD 1, Süleyman Karaagac MD 1, Tobias Schäffter PhD 2, Rolf W. Günther MD 1, Arno Bücker MD 1

1

From the Department of Diagnostic Radiology, University of Technology Aachen, Germany and

2

Philips Research Laboratories, Hamburg, Germany

Running Head:

Pulmonary Embolism: Multi-Modality Comparison

*Correspondence and reprint requests to: Patrick Haage, MD Department of Diagnostic Radiology University of Technology Pauwelsstrasse 30 D-52057 Aachen Germany Phone: 0049-241-80-80303 Fax:

0049-241-80-82302

e-mail: [email protected]

Subject Code for article classification: Thromboembolic disease: diagnosis (90)

Copyright (C) 2002 by the American Thoracic Society.

ABSTRACT In the last decade, Spiral Computed Tomography (CT) and Magnetic Resonance Angiography (MRA) have become a viable alternative to conventional angiography in the diagnosis of acute pulmonary embolism. However, dyspneic patients are often unable to hold their breath for a longer time and thus image degradation is frequently observed. Consequently, a imaging sequence that allows free breathing is desirable. The aim of this animal study was to compare contrast-enhanced Spiral CT, MRA and a real-time MR sequence, the latter without breath-hold, to pulmonary angiography as reference gold standard. Nine pigs with artificially induced pulmonary embolism underwent this multi-modality comparison. All images were independently evaluated for the presence of pulmonary emboli by two reviewers. Forty-three filling defects were detected by conventional angiography on lobar and segmental level. Sensitivity of CT images was 72.1% and 69.8% for reader 1 and 2, respectively, sensitivity of MRA images was 79.1% and 81.4%. With real-time MR imaging, however, the detection rate was 97.7% for both readers. We conclude, that under experimental conditions, real-time MR imaging without the use of radiation or iodinated contrast material is comparable to angiography in the detection of pulmonary emboli.

2

INTRODUCTION Pulmonary embolism (PE) is a frequently observed cause of patient morbidity and mortality. Since this condition has nonspecific signs and symptoms its adequate diagnosis relies on imaging techniques. In case of clinically suspected PE four radiological

modalities

may

be

employed:

conventional

digital

subtraction

angiography [1], contrast-enhanced spiral computed tomography (CT) [2], magnetic resonance angiography (MRA) [3] and real-time MR imaging with radial k-spacescanning [4]. The reference gold standard, conventional pulmonary angiography, is invasive and carries a risk of major complications of 1% and a mortality risk of 0.5% [5] and has thus in many institutions been replaced by spiral CT, which is more readily available with lower procedure-associated risks [6]. Sensitivity of spiral CT is in the order of 90% for central, lobar, or segmental pulmonary emboli [7,8]. MR imaging uses even safer contrast agents than CT and does not involve radiation exposure. In addition, MR imaging allows for the depiction of perfusion and ventilation, which may further aid in the (differential)diagnosis of PE and thus appropriate patient care and treatment [9,10]. This diagnostic technique is improving constantly, and by contrast-enhanced breath-hold techniques pulmonary vessel status can be visualized effectively in most of the cases [11]. Although faster scanning techniques have permitted MRA to be performed in shorter time periods than before, MRA does not yield optimal image quality in people who are unable to hold their breath. A motion compensated projection reconstruction sequence with radial k-space-scanning may offer potential in these patients [12]. Nevertheless, before applying the latter in a clinical setting, its effectiveness in the diagnosis of PE compared to accepted modalities has to be evaluated and confirmed. This was the purpose of the study presented herein; to the best of our knowledge, a comparative

3

analysis of all available modalities including radial real-time MR imaging has not been carried out yet.

METHODS The study protocol was approved by the Animal Care and Use Committee. Handling and caring of the laboratory animals for this study was performed according to state and institutional guidelines.

Thrombus preparation Before commencement of the study, emboli with a diameter of 4 mm were manufactured

by

means

of

a

methyl-methacrylate-based

embedding

resin

(Technovit, Heraeus Kulzer GmbH, Wehrheim, Germany), originally designed for embedding mineralized tissue. The density of the solid resin is comparable to blood and can thus be considered an appropriate model for thrombus detection [13]. This was checked and confirmed by CT at a window width of 360 HU (Hounsfield units) and a center of 80 HU (Figure 1).

PE model The procedures were carried out in nine female pigs with a mean body weight of 40 kg. To avoid infections of the respiratory tract, each animal was treated with a total of four injections of amoxicillin (Duphamox®, AHP AG, Zug, Switzerland) before study initiation. Preceding the procedure, the responsible veterinarian performed a physical examination of the animals. The animals were fasted for 24 hours before the intervention. General anesthesia was induced with intravenous injection of 0.2 ml/ kg body weight azaperone (Stresnil®, Janssen-Cilag, Neuss, Germany) and 0.1 ml/kg body weight 4

ketamine hydrochloride (Ketavet®, Sanofia-Ceva, Düsseldorf, Germany) after intramuscularly applied premedication of 0.05 ml/kg body weight atropine (Atropin®, Braun, Melsungen, Germany). Pentobarbital solution (Narcoren®, Rhone-Merieux, Laupheim, Germany) diluted 1:3 with saline was injected as needed. The animals were intubated and mechanically ventilated with a volume-controlled ventilator (Sulla 808V, Dräger Medizintechnik GmbH, Lübeck, Germany) using a mixture of oxygen, nitrous oxide and halothane (Halothan ASID, Rüsch, Böblingen, Germany). Respirator settings provided a rate of 12 breaths/min and a tidal volume of 500 ml/breath. Throughout the procedure heart rate and blood oxygenation levels were continuously monitored. Under sterile conditions, a 16-F introducer sheath (Kimal, Middlesex, England) was inserted into the right jugular vein and advanced into the proximal superior vena cava over a 0.035 inch J-shaped guidewire with movable core (Cook, Bjaeverskov, Denmark) after access via a surgical cutdown. A total of 50 artificial emboli were then injected through the sheath (range 4 to 6 / animal), which subsequently embolized into the pulmonary arteries.

Pulmonary Angiography After induction of PE, pulmonary arteriography was performed using a commercially available multidirectional Digital Subtraction Angiography Unit (Angiostar Plus, Siemens, Erlangen, Germany) with the pigs placed supine on the imaging platform. Under fluoroscopic guidance a 7 F-Headhunter angiography catheter with 8 sideholes (Cordis, Haan, Germany) was advanced into the main pulmonary trunk over a guidewire. The respirator was turned off at maximum inspiration and pulmonary angiograms were acquired at a rate of 4 frames/second to depict the lung vessel status. Images were obtained in the anteroposterior, right anterior oblique and 5

left anterior oblique projection. 18 ml of a iodinated, non-ionic contrast agent (Solutrast, Altana Pharma , Konstanz, Germany) were mechanically injected through the catheter at a flow rate of 10 ml/s. Further series were recorded after selectively advancing the catheter in the right and left pulmonary artery (10 ml contrast medium, flow rate 4ml/s). After completion of the pulmonary angiogram series the angiographic catheter was removed.

Contrast-enhanced Spiral CT The CT examination was performed with a Tomoscan AV-E1 CT scanner (Philips Medical Systems, Best, The Netherlands) or a Somatom Plus 4 CT scanner (Siemens). 60 ml of the non-ionic contrast agent iopromide (Ultravist 370; Schering, Berlin, Germany) containing 370 mg of iodine per milliliter was administered with a power injector (CT 9000 Digital injection system; Liebel-Flarsheim Company, Cincinnati, OH) via the right jugular sheath. Flow rate was set at 3 ml/sec. After completion of the contrast agent application, 30 ml of sterile isotonic 0.9% saline solution (Delta-Pharma, Pfullingen, Germany) was injected at a rate of 3 ml/sec with a second power injector. Spiral CT scanning was performed with 3-mm collimation, 5mm table increment per gantry rotation (pitch 1.6) and was started 12 seconds after the initiation of contrast material injection to achieve adequate enhancement within the pulmonary arteries during the scan course. The animals were exposed supine in caudocranial direction starting at the end of the diaphragm and extending to the lung apex. Scanning was started in maximal inspiration. Transaxial images were reconstructed at 2-mm increments on a 512 x 512 matrix. A window width of 345 to 360 H and center of 80 H was chosen for all images.

6

Magnetic Resonance Angiography All animals were then studied with a 1.5 T MR imaging system with a maximum gradient amplitude of 23 mT/m/200 ms (Philips ACS-NT, Best, the Netherlands). The experiments were carried out with the animals in the supine position using two synergy surface coils for signal reception. To establish the exact time period required for the contrast bolus to travel from the injection site to the pulmonary arteries, an axial 2D gradient-echo sequence (TR 15 ms ,TE 3 ms, flip angle 75°, matrix 128 x 128, FOV 330 mm, slice thickness 25 mm) was performed at the level of the pulmonary trunk after injection of 2 ml Gd-DTPA. Next, a breath-hold contrastenhanced 3D-MR angiography was performed in coronal slice orientation (TR 4 ms, TE 1.7 ms, flip angle 40°, matrix 256 x 256, FOV 370 mm, slice thickness 2 mm) in maximal inspiration with the respirator turned off after i.v. application of Gd-DTPA (Magnevist, Schering) at a dose and rate of 0.2 mmol/kg body weight and 3 ml/s, respectively. Timing of the intravenous injection was calculated by using the equation: scan delay = contrast travel time + injection time/2 - scan time/2.

Real Time MR Angiography with radial scanning Immediately after completion of the 3D-MRA sequence, radial MR angiography images were acquired. These gradient echo images (TR 16 ms, TE 4 ms, flip angle 18°, slice thickness 4 mm, increment 3 mm, FOV 450 mm, matrix 256 x 256 and 408 radials) were obtained in the axial, coronal and sagittal plane in the same commercially available whole-body 1.5 T MR scanner without additional application of Gd-DTPA. A combination of radial scanning and the sliding window reconstruction technique [14] was applied, in which a dedicated backprojector (Philips Research Laboratories, Hamburg, Germany) allowed for enhanced temporal resolution and thereby data reconstruction in real-time with a frame rate of 20 images per second. 7

This technique, also called view sharing or echo sharing, uses partly old and partly new data to compute the next frame, yielding a higher frame rate and better motion artifact suppression compared with the acquisition of one completely new MR image [15]. Image slice position, orientation, and contrast parameters can be changed interactively, if necessary.

Image interpretation and data analysis Interpretation of the conventional angiographic images was done in a consensus reading by two radiologists who were unaware of the experimental setup and amount of emboli in each pig. The CT images as well as both MR scans were independently assessed by two radiologists. All images were read in random order and were evaluated with hard copies and on a workstation using cine projections. Each reader recorded the intravascular location and number of filling defects. Non-visualization of a vessel alone was considered insufficient evidence for the diagnosis of PE. The accuracy of the reviewers’ diagnoses for all three imaging techniques (spiral CT, MRA, real-time MRA) was calculated. This incorporated detection of embolic defects that were not present (false positive) or their failure to identify emboli that were present (false negative). These results were matched up to the conventional angiography results, which served as the reference method. The sensitivity and positive predictive value of each imaging modality, as interpreted by each reader, was calculated. Since it is not possible to reliably measure the total number of unaffected vessels, the specificity (percentage of true negatives) was not determined. Assessment of differences in the detection rate for thrombi between spiral CT, MRA and real-time MRA was done by the unpaired two-tailed Student t-test. Probability (p) values were calculated for each comparison based on a significance level of 0.05.

8

Interobserver agreement was evaluated with the use of the kappa statistic, where k is 1 in case of perfect agreement, k is 0 if there is no agreement better than chance and k is negative when agreement is worse than chance [16].

RESULTS The surgical and experimental protocol was technically successful in all nine animals. Except for one case of transient tachycardia directly after PE induction, no significant changes in vital signs were observed. Forty-three out of the 50 emboli migrated from the superior vena cava into the pulmonary arterial tree, 7 got trapped in the right atrium. The average duration of anesthesia was 6 hours. No episodes of adverse contrast medium reactions were noted. All conventional angiography (Figure 2) and CT (Figure 3) images were of diagnostic quality and could be included in the evaluation. Lung vessels could also be effectively depicted with the MRA sequence (Figure 4) and the real-time radial MR sequence (Figure 5) down to segmental and to some extent subsegmental level. Artificial thrombi were found in lobar and segmental arteries in all pigs. Forty-three affected

vascular

territories

were

counted

by

conventional

angiography.

Corresponding to the size of the emboli all filling defects were contained on lobar or segmental level. Subsegmental vessels were patent and free of thrombus due to their lesser diameter. 51.2 % of the thrombi were localized on the right side, 48.8 % on the left. Sixteen of the 43 (37.2 %) emboli were detected in lobar arteries, the remaining 27 had advanced into segmental arteries. The sensitivity of spiral CT images was 72.1 % for reader 1 and 69.8 % for reader 2 (mean 71.0 %), sensitivity of MRA images was 79.1 % for reader 1 and 81.4 % for reader 2 (mean 80.3 %).

9

The analogous value for the real-time MR images was 97.7 % for the two readers, who both detected all emboli except for one left-sided segmental embolus. False positive diagnoses were not observed with either modality yielding a positive predictive value of 100%. Differences in the detection rate for emboli between spiral CT and MRA (p = 0.06) and between MRA and real-time MRA (p = 0.14) to determine the level of confidence were not statistically significant. Only the difference between spiral CT and real-time MRA was of statistical significance (p = 0.01). The inter-rater coefficient k was 0.86 for CT, 0.84 for MRA and 1.0 for real-time MRA.

DISCUSSION The results of the presented study show that in this pig model, real-time MRA with radial scanning is comparable to conventional pulmonary angiography with better performance than contrast-enhanced spiral CT and MRA for the visualization of pulmonary emboli. All investigated modalities have demonstrated good to excellent interobserver agreement. Clinically, requirements of an acceptable PE assessment are that it is feasible in most patients and leads to the proper diagnosis and consecutively, the appropriate therapy. To this regard, angiography has long been recognized to be the most exact modality with a sensitivity and specificity of 95% and 100%, respectively [5,17]. Thus it is considered the reference standard, that all other techniques have to be measured against. Advantages include the option of inducing a local fibrinolysistherapy via the angiographic catheter already in place. However, angiography is not possible in up to 20% of patients and due to its associated invasiveness, morbidity and sporadic mortality it is nowadays being employed less frequently and replaced by spiral CT and recently MRA, both of which are faster, less invasive, less operatordependent and are associated with a smaller number of complications [5,18]. 10

Another advantage of Spiral CT is its widespread availability. Conversely, MRA has advantages over spiral CT, because it does not involve ionizing radiation and it makes use of smaller amounts of gadolinium chelates, which have an even better safety profile than iodinated contrast agents [19,20]. Over the last few years many of the limitations of earlier MR techniques were dealt with. High signal-to-noise ratios and high contrast between flowing blood and pulmonary filling defects can now be depicted with the development of contrastenhanced MRA in a single breath-hold, during "first-pass" imaging with Gadoliniumcontaining contrast media. The key aspects that restrict magnetic resonance angiography application are non-diagnostic quality of images and alterations that avert a patient from entering a magnetic field, which together are in the order of 15% [21]. These difficulties are a weakness of MRA, particularly when compared with spiral CT. Furthermore, the necessity to eliminate the need for breath-holding for the detection of pulmonary emboli in dyspneic patients is beyond question for any imaging modality. Improved gradient performance, ultrafast reconstruction capabilities [22], and lately developed software tools for "on-the-fly" interactive MR scanning [23] now offer the potential for real-time MR imaging with satisfactory contrast and spatial resolution for pulmonary MRA. Herein, radial MRA showed a high contrast of the pulmonary artery lumen. Enhanced motion artifact suppression was achieved by combination of the real-time data acquisition with radial k-space filling, which offers better motion artifact suppression when compared with cartesian readouts [14,24]. An additional advantage of radial k-space filling is an option for undersampling of radials, thereby further enhancing temporal resolution without sacrificing spatial resolution [25]. Consequently, in contrast to cartesian k-space filling, the radial acquisition spatial 11

resolution is not negatively affected by time-saving undersampling. In addition, improved temporal resolution was achieved applying the sliding window technique [26]. The present study was designed to assess the applicability of real-time MRI techniques in an established animal model, wherein the technique combination allowed for high-quality pulmonary vessel visualization, exploiting the continued shortening of T1 due to the injected contrast agent. Bolus tracking for timing of the arterial contrast medium passage was not necessary. Mean image acquisition time was 9 minutes, whereby uncertain vascular territories, contrary to spiral CT and MRA, could be repeatedly evaluated. The high frame rate permitted data acquisition during free breathing and without cardiac triggering. Albeit the results show that real-time MRA is comparable to pulmonary angiography for the detection of pulmonary emboli in this animal model, some restrictions as to experimental setup must be reflected on before the results can be transposed to a clinical setting. These include differences between species that might influence lung anatomy as well as the use of artificial methyl-methacrylate thrombi rather than “real” thrombi, which can only approximate the clot seen in clinical pulmonary embolism. The pulmonary anatomy and vessel size of the pig are not identical to the human anatomy with one large main pulmonary arterial trunk with many smaller arteries rather than the dichotomous branching configuration of the human pulmonary vascular tree [27]. The emboli were prepared so that they would migrate and lodge in branches of the major artery which are approximately the same size as human subsegmental pulmonary arteries [13]. The sensitivity values should not have been affected by differences in anatomy, since there is no rationale that these differences between pigs and humans should lead to improved accuracy of one technique. Principally, the use of real blood clots as thrombi would have been an ideal 12

thrombosis model, but the comparability of different modalities requires constant size and position of the filling defects over at least several hours, which would not have been possible with real thrombi. The lower sensitivity values of spiral CT in our setup will certainly improve with the advent of multi-slice spiral CT [28]. At this time, due to its availability and speed, spiral CT should still be considered the preferred diagnostic modality in suspected pulmonary embolism [29], in particular if or as long as ICUpatients are treated with non-MR-compatible equipment. In conclusion, it is not proposed that real-time MRA can be used to definitely rule out PE. The results however demonstrate its advantages and potential in comparison to CT and “conventional” MRA. Real-time radial MR scanning allows promising image acquisition of the pulmonary vasculature without respiratory control. Especially severely dyspneic patients may profit from this imaging modality, since real-time imaging

quality

is

not

degraded

by

respiratory

motion.

Further

technical

improvements and clinical evaluations are warranted before applying this technique as an alternative to already established modalities in the diagnostic approach to pulmonary embolism.

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TABLE 1

Sensitivity (%) of Spiral CT, MRA and real-time MRA for detecting pulmonary emboli

Sensitivity (%) Reader

CT

MRA

RT-MRA

1

72.1

79.1

97.7

2

69.8

81.4

97.7

Overall mean

71.0

80.3

97.7

k

0.86

0.84

1.0

Definition of abbreviations: RT-MRA = Real-Time MRA, k = interobserver agreement.

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Figures

Figure 1. Photograph of the methyl-methacrylate thrombus (A) and blood clot (B) and respective CT-depiction (C and D).

A

B

Figure 2. Conventional pulmonary angiography demonstrates the bilateral peripheral emboli in the lower lobe arteries (A) with corresponding perfusion defects (B).

19

A

B

Figure 3. Emboli are easily visualized with contrast-enhanced spiral-CT (A,B; arrows) in the same animal as Figure 2.

A

B

C

Figure 4. 2 mm coronal MRA slices in the same animal as Figure 2 and 3 show bilateral emboli after i.v. contrast medium application (A,B,C; arrows).

20

A

D

B

C

E

F

Figure 5. Delineation of thrombi in axial, sagittal and coronal orientation (A-F; arrows) with real-time radial MRA, again in the same animal as Figures 2-4.

21