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Original Research |
1 Department of Diagnostic Radiology, Kerckhoff Heart Center, Beneke-Strasse
2-8, 61231 Bad Nauheim, Germany.
2 Department of Rheumatology, Kerckhoff Heart Center, Bad Nauheim,
Germany.
Received May 3, 2005;
accepted after revision August 12, 2005.
Address correspondence to A. Kluge.
Abstract
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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SUBJECTS AND METHODS. Two hundred twenty-one consecutive patients (119 men, 102 women; mean age, 51 years; range, 31-86 years) with suspected PE were examined using a multitechnique thoracic MRI protocol (real-time MRI using true fast imaging with steady-state precession [FISP], perfusion MRI, and MR angiography) followed by stepping-table MR venography.
RESULTS. Two hundred twenty-one thoracic MRI examinations were
performed. Two hundred eighteen MR venography examinations were scheduled, of
which five (2.3%) were not performed for clinical or technical reasons and six
were not performed after negative thoracic MRI. Among 207 combined
examinations, PE was diagnosed in 76 and DVT in 78 examinations. Thirteen
patients without PE showed DVT; thus, MR venography detected 17% additional
cases of thromboembolism. Agreement with duplex sonography was good at the
upper leg (
= 0.87-0.89) but moderate at the pelvis ( =
0.59-0.65).
CONCLUSION. A combined "one-stop-shopping" MRI approach for PE and DVT was routinely feasible and detected 17% more cases of thromboembolism compared with separate examinations. MRI may be considered a second-line technique to avoid contraindications to CT but also a primary comprehensive technique for diagnosing thromboembolism.
Keywords: cardiopulmonary imaging • cardiovascular disease • deep vein thrombosis • embolism • MRI • venography
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Currently, widespread expertise and availability and its high sensitivity and specificity make helical CT angiography the most often used technique for diagnosing PE [3-5]. To diagnose DVT in suspected thromboembolism, duplex sonography, CT venography, and fluoroscopic ascending venography are applied. CT allows the execution of a "one-stop-diagnostic" for PE and DVT [2, 6]. However, the radiation exposure is substantial [7], and CT venography notably increases the gonadal dose [8, 9].
One of the most important advantages of MRI in this context is the absence of radiation exposure. However, MRI has played a rather restricted role in the diagnosis of PE because of its long examination time and limited patient access. Recent developments, though, have shown the capability of MRI for emergency thoracic diagnostics [10, 11] and for the diagnosis of PE in noncooperative patients [12]. The sensitivity of MR angiography for the detection of PE ranges from 84% to 100% [13], and pulmonary perfusion MRI shows high agreement with SPECT and CT angiography [14-16]. A combination of direct and indirect MRI techniques for the diagnosis of PE (real-time MRI, MR angiography, and pulmonary perfusion MRI) allows an increase in sensitivity and specificity [17]. Indirect MR venography [18] depicts the entire venous system of the lower limb and detects DVT with a sensitivity and specificity that matches fluoroscopic venography, and vessel coverage is superior [19].
A prerequisite for a combined MRI examination of both the thorax for suspected PE and the legs for suspected DVT is a fast imaging protocol: MRI examination times as short as 3-10 min for the diagnosis of PE [12, 17] and 6-10 min for the diagnosis of DVT have been shown to be achievable on a routine basis without any interference by earlier contrast media application for thoracic MRI on MR venography [19]. Thus, a combined MRI examination of the thorax and the legs should be feasible. Such a combined MRI diagnostic procedure has not yet been published.
We therefore attempted a study with four objectives in mind: first, to assess the logistic and technical feasibility of a combined protocol for the diagnosis of PE and DVT in clinical patients, emphasizing examination time and the patient's clinical situation; second, to assess the quality of each component of the combined MRI examination and to quantitatively evaluate MR venography images acquired directly after contrast-enhanced thoracic MR images; third, to assess the rate of patients with thromboembolic disease—that is, to evaluate the rate and significance of DVT in patients negative for PE and vice versa to assess the additional value of a comprehensive examination compared with single-organ examinations; and fourth, to evaluate the intertechnique agreement of MR venography and duplex sonography.
Subgroups of patients enrolled in our study participated in two published studies. These studies reported the diagnostic accuracy and technical aspects of MRI for the diagnosis of PE compared with 16-MDCT [17] and for the diagnosis of DVT compared with fluoroscopic venography [19]. In contrast, our study focuses on the feasibility and results of a combined MRI protocol for PE and DVT, with an emphasis on feasibility and the distribution of PE and DVT. No data were duplicated.
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The inclusion criterion was the suspicion of an acute PE. The suspicion of PE arose from clinical symptoms and from ECG and echocardiography performed in all patients. The results of a D-dimer test were available for 97 patients (mean, 752 ng/mL; range, 180-6,000 ng/mL; reference value, < 200 ng/mL). Exclusion criteria for the MRI examination were cardiogenic shock or prolonged low cardiac output (systolic arterial pressure < 60 mm Hg), and an implanted device. Following these criteria, two patients with a cardiac pacemaker were not enrolled. Patients were classified as showing either no or mild dyspnea (138 patients), marked dyspnea or agitation (58 patients), and severe dyspnea or decreased systolic blood pressure (25 patients) [20].
The study was approved by the local ethics committee, and informed consent was obtained from all patients.
Study Protocol
The study protocol required thoracic MRI for the diagnosis of PE followed
by MR venography for the diagnosis of DVT. The diagnostic precision of the
thoracic MRI protocol was previously compared with 16-MDCT angiography, the MR
venography technique was compared with fluoroscopic venography, and results
have been published [17,
19]. For this reason, the
study protocol did not require a reference standard. In fact, the study
population included patients participating in studies of the diagnostic
accuracy of MRI, so that subgroups of patients underwent reference
examinations, the distribution of which is given in
Table 1. MRI was available both
day and night. CT was performed not longer than 1 hr before or after MRI;
duplex sonography was performed before MRI; and fluoroscopic venography, after
MRI.
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MRI Protocol
The following MRI protocol was followed as long as the clinical situation
of the patient permitted it. If the protocol had to be aborted, diagnosis was
made on the basis of sequences completed by that stage. The examination could
be stopped after real-time MRI if an acute thoracic disease fully explaining
the patient's condition was detected without any sign of PE, and if no further
diagnostics were required. Thoracic MRI was performed first, followed by MR
venography.
Thoracic MRI—The protocol for pulmonary MR diagnostics consisted of three parts, with the most robust techniques applied first, followed by techniques for more subtle diagnostics in patients who tolerated longer imaging times: real-time MRI for emergency imaging, perfusion MRI, and contrast-enhanced MR angiography. Detailed parameters have been published [17]. The MRI examination started with the patient lying in the supine position on the examination table, with his or her head oriented toward the magnet. A six-segment phased-array body coil was placed on the patient's chest, supplemented by corresponding segments of the table's array coil. Contrast material was applied through a peripheral venous access (a 20-gauge needle in an antecubital vein) with a power injector (Spectris, Medrad). No ECG was routinely performed because no cardiac-gated sequences were applied.
Thoracic MRI: real-time MRI—With nonsegmented true fast imaging with steady-state precession sequences (true FISP, balanced fast-field echo, FIESTA [fast imaging employing steady-state acquisition]), 320 50%-overlapping images were acquired in three orthogonal planes and covered the entire thorax from the pulmonary apex to the hepatic portal vein. Predefined oversized imaging areas superseded an individual adaptation of slice position or sequence parameters. Sequence parameters were TR/TE, 3.1/1.5; flip angle, 59°; bandwidth, 1,000 Hz/pixel; slice thickness, 3-4 mm; field of view, 340-360 mm; matrix size, 156-192 x 256 pixels; and an acquisition time of 0.4-0.52 sec per slice. Every segmental vessel was depicted in three orientations on at least two images per orientation. Motion artifacts could occur only during the acquisition time of 0.5 sec per image, so that the sequences were in fact robust to motion artifacts.
Thoracic MRI: pulmonary perfusion MRI—A 3D FLASH (fast low-angle shot) sequence was used: 1.6/0.6; flip angle, 25°; bandwidth, 1,500 Hz; matrix size, 256 x 128-192; 20 transverse partitions of 10-mm thickness; field of view, 400 x 200-300 mm (depending on the patient's thoracic diameter). The voxel size was 2.9 x 1.6 x 10 mm, and a typical acquisition time was 1.6-1.7 sec. Gadopentetate dimeglumine, 0.125 mmol/kg of body weight, was injected at 4 mL/sec at the start of the sequence. Twenty-five repeated measurements covered the first and second passes of the contrast medium bolus in 45 sec. The lung was covered from the apex to the diaphragm, thus neglecting posterobasal parts of S-10.
Thoracic MRI: MR angiography—A 3D FLASH sequence was started with a second injection of 0.125 mmol/kg of body weight of gadopentetate dimeglumine at 4 mL/sec after a bolus timing sequence (3.2/1.4; flip angle, 25°; field of view, 340 mm; 512 x 384 pixels; 80 coronal partitions; voxel size, 0.7 x 1.2 x 1.5 mm; parallel acquisition with GRAPPA [generalized autocalibrating partially parallel acquisitions]; 24 auto calibration lines; acquisition time, 14 sec).
MR venography—Indirect venography immediately followed thoracic MRI using the contrast media already applied for the thoracic MRI examination. The patient was moved to an MRI-safe couch using a transfer mattress, the couch was turned around, and the patient was repositioned feetfirst on the examination table. The infusion line and the phased-array coil were removed and a peripheral angiography phased-array coil was attached, and a quadruple phased-array coil was placed on the patient's pelvis and abdomen.
Detailed parameters of the MR venography protocol (also 3D FLASH) have been published previously [19]. After scout views, the lower leg, including the calf; upper leg; and pelvis were imaged in that order using an automated stepping-table protocol. The lower limb was covered from the malleolar region to the inferior vena cava 10 cm proximal to the bifurcation. Sequence parameters were 4.36/1.49; flip angle, 30°; bandwidth, 270 Hz; matrix, 512 x 207; voxel size, 1.2 x 0.8 x 1.1 mm; 80 partitions; fat saturation; parallel acquisition; acquisition time, 20 sec. The pelvic region was visualized without parallel acquisition for better signal-to-noise-ratio (SNR): 2.5/0.98; flip angle, 20°; bandwidth, 690 Hz; matrix, 384 x 200; voxel size, 1.7 x 1.0 x 1.5 mm; 80 partitions; fat saturation; acquisition time, 19 sec. No contrast medium was administered after the patient was repositioned.
Duplex Sonography
Duplex sonography was performed the day before MRI was scheduled,
independently of the MRI examination, at the discretion of the treating
physician, and data were collected retrospectively. The veins from the
popliteal fossa to the external iliac vein were examined, and indirect signs
of pelvic vein thrombosis were evaluated using established criteria for DVT
[21]: visualization of
thrombus, absence of spontaneous flow on Doppler sonography, absence of
phasicity of flow with respiration, and incompressibility of the vein on probe
pressure. The examination of the lower leg was not performed in all
patients.
Evaluation
The first study objective was to assess the feasibility of combined
thoracic and venography MRI examinations. Therefore, protocol adherence was
evaluated with patients grouped by clinical condition. If the protocol was not
completed, images collected to that point were graded as either sufficient or
inadequate for making a diagnosis. The MRI examination time was determined by
the DICOM tags for acquisition time as well as the series and imaging
times.
The second objective was to assess the technical quality of such a combined examination, which was done separately for each MRI technique. Diagnostic quality of real-time MRI and MR angiography sequences was assumed when no more than three lobar arteries or 10 segmental arteries could not be evaluated. For perfusion MRI, signal intensity (SI) sufficient to distinguish perfusion defects from normal lung tissue was required. The diagnostic quality of MR venography required vessel contrast, allowing thrombotic material, filling defects, and surrounding tissue to be distinguished. Vessel coverage was assessed for 13 vein groups (six per side: deep lower leg veins with the popliteal vein, perforating vein, and muscular veins; superficial lower leg veins; deep upper leg veins; superficial upper leg veins; iliac veins; and the inferior vena cava). To calculate SIblood/thrombus and SNR of blood and thrombotic material (SI/noise) and contrast-to-noise ratio (CNR) of thrombus versus blood [(SIblood-SIembolus)/noise)], regions of interest (ROIs) encompassing more than 16 pixels were placed in the external iliac vein, in the superficial femoral vein at the canalis adductorius, in tibial veins, and in thrombotic material.
The third study goal, to evaluate combined MRI examinations for the detection of thromboembolic disease compared with thoracic MRI and MR venography alone, was assessed by comparing the numbers and locations of thrombotic material for each combination of positive and negative findings for PE and DVT.
The fourth objective, the intertechnique agreement with duplex sonography, was retrospectively calculated both on a per-thrombosis basis for the upper leg and pelvic veins (duplex sonography was performed from the popliteal fossa upward) and on a per-patient basis. To compare the rate of findings between MR venography and duplex sonography, every region not mentioned as positive for DVT was classified as negative for DVT.
Image Analysis
All images were interpreted in a fixed order of sequence types in a
consensus interpretation by two experienced radiologists who were unaware of
the results of clinical data, previous tests, or other MRI sequences. Raw
images were used with additional multiplanar reconstructions but without any
maximum intensity projection for MR angiography and MR venography. Criteria
for PE on real-time MRI and MR angiography were direct thrombus visualization
or vessel cutoff, which are analogous to criteria for conventional pulmonary
angiography and CT angiography. For real-time MRI, concordant results from two
planes were required. The proximal inferior vena cava was evaluated for
thrombosis on coronal real-time images. On perfusion MR images, sharply
delineated perfusion defects were defined as PE if contours were consistent
with segmental or subsegmental anatomy. Multilocalized patchy perfusion
attenuations were defined as chronic obstructive pulmonary disease (COPD).
Diagnosis was verified by spirometry and medical records.
The most central embolus location determined the extent of PE (real-time MRI: central, lobar, or segmental; MR angiography and perfusion MRI: central, lobar, segmental, or subsegmental). A final consensus interpretation of all three thoracic MRI techniques was performed if a discrepancy between the MRI techniques was evident. As such, false-positive findings were at first excluded (e.g., fibrous pulmonary scar mimicking PE on perfusion images, but being visualized as scars on real-time MRI; or anatomy, atypical branching, or flow artifacts on real-time images mimicking segmental PE with perfusion and MR angiography remaining normal). Then false-negative findings were excluded (e.g., sharply defined subsegmental perfusion defects visualized with perfusion MRI, but not visualized with MR angiography because of limited spatial resolution; or lobar recanalized PE visualized with MR angiography and real-time MRI, although only multisegmental PE is visualized with perfusion MRI because of undisturbed lobar perfusion).
The criterion for DVT was direct visualization of hypointense thrombotic material in a vein. Thrombus was categorized as lower leg DVT, upper leg DVT, muscular vein thrombosis, or pelvic vein thrombosis.
Concomitant findings were sought on images of thoracic MRI and MR venography. Findings were then compared with medical history and records. If required, additional examinations were performed to confirm or rule out MRI findings. Aortic dissections were also examined with cardiac-gated MRI sequences and MR angiography of the aortic arch so that entry and reentry could be better visualized.
Statistical Analysis
Frequencies were compared using the Kruskal-Wallis test, and intertechnique
agreement for DVT was calculated using Cohen's kappa values for vascular areas
assessed with both duplex sonography and MR venography—that is, the
pelvis and the upper leg.
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MR venography was intended for 218 patients but was performed in only 207 patients (95%). The patient's clinical condition (four patients) and technical reasons (one patient) precluded MR venography in 5 (2.3%) of the 218 patients. Request by the patient or referring physician to end the protocol on hearing the negative findings of thoracic MRI occurred in six cases, so uncertainty concerning the examination was not a factor. Relevant motion artifacts did not occur, and image quality and vessel contrast were considered sufficient in all patients. Hip or knee replacement prosthetics caused artifacts that precluded analysis of directly adjacent vessels, but not the entire vascular region.
The mean time from the beginning of the patient positioning (t0) to the completion of each protocol step was as follows: positioning of the patient, coil connection, and shimming, 1 min 8 sec ± 21 sec; real-time MRI, 3 min 55 sec ± 3 sec; test bolus and perfusion MRI, 7 min 6 sec ± 15 sec; MR angiography, 8 min 40 sec ± 24 sec; and patient repositioning for MR venography, 11 min 58 sec ± 28 sec. Thus, the repositioning of the patient to the feetfirst position and the changing of the coils required 3 min 18 sec. Completion of image reconstruction then had to be waited for, MR venography started 13 min 39 sec ± 31 sec after t0, and MR venography was completed after 19 min 41 sec ± 28 sec.
The mean signal intensity of blood was 106.2 ± 11 at the lower leg, 60.4 ± 18.9 at the upper leg, and 52.4 ± 16.5 at the external iliac vein. Mean signal intensity of thrombotic material at all levels was 12.3 ± 5.2 (range, 6-19). The signal intensity ratio of blood and thrombus amounted to 8.1 ± 0.5 at the lower leg, 5.5 ± 0.6 at the upper leg, and 3.7 ± 0.4 at the external iliac vein. The mean SNR of blood on MR venography was 19 ± 9 in pelvic veins, 22 ± 8 at the upper leg, and 20 ± 7 at the lower leg. CNRblood/muscle values at the respective locations were 13 ± 8, 15 ± 8, and 14 ± 7. Corresponding values for CNRblood/thrombus were 15 ± 11, 17 ± 12, and 16 ± 10.
Of 13 venous vascular regions examined in 207 examinations, all iliac veins, all deep upper leg veins, and all deep lower leg veins were visualized. The inferior vena cava was visualized in 202 (97.6%) of 207 examinations; 205 right (99.0%) and 206 left superficial upper leg veins (99.5%), 196 lower leg superficial veins (94.7%) on each side; and 201 (97.1%) muscular veins on the right and 202 (97.6%) on the left were imaged. Thus, 2,652 (98.6%) of 2,691 vascular regions were visualized.
Distribution of Thromboembolic Disease
PE was diagnosed in 79 of 221 patients examined. Of 14 patients who did not
undergo MR venography, PE was diagnosed in three patients. For 207 patients
who underwent both thoracic MRI and MR venography, the distribution and
concurrence of PE and DVT are shown in Tables
3 and
4. Figure
1A,
1B,
1C,
1D,
1E and
1F shows typical findings of PE
and DVT, and a case of extended DVT is shown in
Figure 2. The frequency of
occurrence and the distribution of PE differed between patients with and those
without DVT (p < 0.00001), and the frequency of occurrence and
distribution of DVT differed between patients with and those without PE
(p < 0.00001). On the other hand, distribution of present PE
between patients with and those without DVT did not differ significantly, and
distribution of present DVT did not differ significantly between patients with
and those without PE. The addition of MR venography detected 13 more patients
with thromboembolic disease than thoracic MRI alone (13/76, 17.1%), and the
addition of thoracic MRI detected 11 more patients with thromboembolic disease
than MR venography alone (11/78, 14.1%).
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MR Venography Versus Duplex Sonography
Fifty-three patients underwent both MR venography and duplex sonography. MR
venography detected DVT in 22 patients, and duplex sonography, in 15 patients.
In addition, MR venography detected two patients with thrombosis in pelvic
veins, one patient with upper leg DVT, and four patients with lower leg DVT.
Thrombosis of the inferior vena cava in two patients was detected on real-time
MR images (Figs. 3A,
3B) but not with MR venography
or duplex sonography. Table 4
shows the per-thrombus comparison of DVT.
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Regarding the study objectives, the feasibility of combined MRI examinations for PE and DVT incorporating direct and indirect visualization of PE and MR venography was shown. Clinical or technical reasons precluded the intended combination in only five examinations (2.3%). The robustness of the thoracic MRI protocol is due to the concurrence of a severe clinical condition with pronounced findings that present no great problems for detection, whereas subtle findings that require more detailed diagnostics are associated with a better clinical condition [12, 17]. For that reason, the thoracic protocol allowed clinical decision making even when all protocol steps had not been completed. Although real-time MRI, perfusion MRI, and MR venography examinations reached diagnostic quality, the sensitivity of MR angiography to motion artifacts in more severe stages of PE [12, 17] was confirmed. The robustness of MR venography was credited to fact that respiratory movements had little effect on the pelvis and legs. The technical quality of MR venography in the combined protocol confirms previous findings showing the importance of contrast medium dose and the tolerance to contrast medium timing [19]. Furthermore, postprocessing did not depend on proper sequence registration in the same way, for example, that subtraction-based analysis does.
The addition of MR venography to thoracic MRI revealed 17.1% more patients with thromboembolic disease, of which four had upper leg DVT. The combination of a stepping table and parallel acquisition allowed rapid acquisition while maintaining complete coverage of the pelvic and lower limb venous system. Previous studies have underlined this diagnostic yield, in which an additional 14-36% of patients were revealed with thromboembolic disease when CT venography was added to CT angiography [2, 6, 22]. The combined MRI protocol required less then 10 min for this diagnostic step, obviating additional and separate leg diagnostic procedures that might delay the final diagnosis.
The comparison of duplex sonography with MR venography reflected the better vessel coverage for the latter when, for example, calf veins are routinely included in the examination. Intertechnique agreement was very good at the upper leg level but only moderate at the pelvic level; this was because of the detection of seven additional pelvic vein thromboses by MR venography. This finding is consistent with the previously reported diagnostic accuracy of duplex sonography at the pelvic level [23, 24]. Although MR venography repeatedly showed high sensitivity and specificity [18, 19, 25], duplex sonography as performed in our study was adequate for detecting most clinically significant DVT but was not suitable for ruling out thromboembolic disease. Vessel coverage appears to be all the more important because DVT at locations usually regarded as not clinically significant has been shown to have an impact on clinical outcome [26].
The importance of MRI compared with other imaging techniques for diagnosing thromboembolic disease is yet to be clarified. CT angiography is the predominant imaging technique for diagnosing PE [3, 4] and is increasingly being combined with CT venography [2, 6, 27, 28]. The MRI protocol avoids two disadvantages of CT: The significant radiation exposure with CT [7-9, 29, 30] is no longer a problem, and the entire deep venous system, including the lower leg, is covered, which is not the case with normal CT venography. Although no direct comparison of CT venography and MR venography has been published, and SNR and CNR are not available for most CT venography studies, the SI ratiothrombus/blood can serve to substitute for vessel-thrombus contrast. Values ranging from 1.8 to 3.2 can be calculated for CT venography [27] compared with values from 3.7 to 8.1 in this study.
Furthermore, MRI has a number of specific advantages: Follow-up examinations in patients with acute PE are feasible [31] and allow monitoring of pulmonary function under therapy. Although both CT and MRI allow detection or exclusion of thoracic disorders mimicking PE [10-12, 17, 28, 32, 33], complementary cardiac MRI can be added immediately to assess the functional impact of the disease.
The direct quantification of embolus load is of prognostic relevance [34, 35], and a future comparison with the prognostic significance of indirect, functional parameters visualized on perfusion MRI would appear to make sense: The impact of embolus recanalization and lysis on right-heart load and blood oxygenation may be scored differently with direct and indirect PE visualization techniques. An outcome study should therefore be performed to assess the clinical significance of the additionally detected thromboembolic diseases of lower leg thrombosis and superficial vein thrombosis.
Some limitations of this study must be noted. The combined MRI approach has not been directly compared with the combination of CT angiography and CT venography. However, as mentioned, the diagnostic accuracy of thoracic MRI has been compared with CT angiography [17], and MR venography has been compared with the accepted reference standard, fluoroscopic venography [19]. Our study is a single-center nonrandomized study, and data for the comparison of duplex sonography and MR venography are based on a retrospective analysis in a minority of the study population.
In conclusion, the combination of multitechnique thoracic MRI for PE and MR venography for DVT was feasible in less than 20 min on a routine basis, thus enabling a one-stop-shopping approach to diagnose or exclude acute thoracic diseases and DVT. Because patient cooperation is not required, the protocol can be applied in the normal clinical routine in the our radiology department. Because of our results, clinical guidelines in our institution now accept thoracic MRI as the primary diagnostic technique for suspected PE and MR venography of the legs in patients with suspected PE who are already scheduled for MRI of the thorax.
The combined MRI protocol presented here may be regarded as a first step for the development of alternatives to established comprehensive CT protocols, with disadvantages inherent to CT being avoided and additional advantages becoming apparent—that is, the assessment of pulmonary perfusion and the better vessel coverage for diagnosing DVT.
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