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Vascular and Interventional Radiology |
1 Department of Radiology, Sir Charles Gairdner Hospital, Queen Elizabeth II Medical Centre, Verdun St, Nedlands 6009, Western Australia.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Thirty-six consecutive patients (19 women, 17 men; age range, 28–84 years) underwent pulmonary digital subtraction angiography (DSA) and pulmonary MR angiography. MR angiograms were obtained during suspended respiration and the pulmonary arterial phase of a gadolinium-based contrast medium injection. A steady-state gradient-recalled-echo sequence with free induction decay sampling was used. DSA studies were interpreted for the presence of acute PE by two independent radiologists; an adjudicator made the final decision on discordant interpretations.
RESULTS: By using DSA, a total of 19 acute pulmonary emboli were depicted in 13 patients. Prospectively, 13 of these emboli were depicted by using MR angiography. MR angiography missed six emboli: Four required the DSA adjudicator to make the decision, and one was in a patient whose MR angiogram was acquired during breathing. Four of these six emboli were small subsegmental emboli, and two were segmental.
CONCLUSION: Performed without pulmonary arterial catheterization, iodinated contrast media, or ionizing radiation, pulmonary MR angiography had a high accuracy for depicting lobar and segmental emboli, but was unable to depict four of five subsegmental emboli.
Index terms: Embolism, pulmonary, 564.783, 944.77 • Magnetic resonance (MR), angiography, 564.12142, 944.12942 • Magnetic resonance (MR), comparative studies • Pulmonary angiography, 564.12142, 564.124, 944.1222, 944.12942 • Pulmonary arteries, stenosis or obstruction, 564.783, 944.77
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Because the clinical history and examination findings are nonspecific, acute PE frequently is undiagnosed. Goldhaber et al (3) reported that of 54 patients with anatomically important PE at autopsy, 16 (30%) had a correct antemortem diagnosis; the diagnosis had been missed in all 21 patients with coexisting pneumonia.
The diagnostic examination frequently requested is ventilation-perfusion (V-P) scanning. However, the Prospective Investigation of Pulmonary Embolism Diagnosis (PIOPED) investigators (4) concluded that V-P scanning combined with clinical assessment enabled the noninvasive diagnosis or exclusion of acute PE in a minority of patients.
Percutaneous catheter pulmonary angiography is the present standard method of reference, but it is associated with minimal but definite morbidity and mortality (5); thus, many clinicians are reluctant to refer patients for pulmonary angiography, even when there is diagnostic uncertainty. A noninvasive and accurate diagnostic examination that directly depicts the pulmonary arteries and pulmonary emboli is clearly needed.
The purpose of our study was to assess the capability of magnetic resonance (MR) angiography in the diagnosis of PE by using the latest technology of breath-hold imaging with a fast gradient-recalled-echo sequence, a short repetition time and echo time, and gadolinium-based contrast medium enhancement.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Pulmonary MR Angiography
All pulmonary MR angiograms were obtained by using a 1.5-T Vision MR imaging system (Siemens Medical Systems, Erlangen, Germany). The body coil was used for signal transmission. A circularly polarized phased-array torso coil that encompassed the thorax was used for signal reception. A three-dimensional fast imaging with steady-state precession sequence (Siemens Medical Systems) was used. This is a steady-state gradient-recalled-echo sequence with fast induction decay sampling. The imaging parameters were as follows: 5/2 (repetition time msec/echo time msec), 25° flip angle, 108-mm section thickness, 32 partitions, 140 x 256 acquisition matrix, 35 x 35-cm field of view, 2.5 x 1.4 x 3.4-mm voxel size, and 23-second acquisition time. In thin patients, a rectangular field of view was used. This reduced the field of view to 30.6 x 35.0 cm and the acquisition time to 20 seconds; the proportion of the lung fields within the imaging volume was unaffected. Cardiac gating was not used because of the resultant increase in acquisition time.
A peripheral intravenous line was placed in an antecubital vein and was connected by using 51-cm tubing (Extension Set; Baxter, Deerfield, Ill) to a 20-mL syringe that contained gadodiamide (Omniscan; Nycomed, Oslo, Norway). Lying supine and with the arms extended above the head, the patient was placed head first into the bore of the magnet.
Localizing images, which were used for positioning the imaging volume, were obtained in suspended expiration by using the following gradient-recalled-echo sequence: 15/6, 30° flip angle, 10-mm section thickness, five sections, 128 x 256 acquisition matrix, 45 x 45-cm field of view, and a 16-second acquisition time. The imaging volume was positioned in a coronal oblique orientation, with the superior border placed anteriorly. The posterior aspect was placed at or near the posterior border of the vertebral bodies in the middle region of the thorax.
After hyperventilating for 30 seconds, the patient was asked to suspend respiration at expiration. Then, a 20-mL bolus of gadodiamide was immediately injected manually in approximately 5 seconds followed by a 20-mL saline flush. The imaging sequence was then started, with a 5-second delay between the start of the injection and the start of the imaging sequence. A physician in the magnet room gave the breathing instructions and injected the gadodiamide. A radiographer in the control room manually started the imaging sequence. An intercom system was used for communication. With the image having been acquired, the patient was asked to breathe for 5 seconds and then suspend respiration as before, and the imaging sequence was repeated without an additional administration of gadodiamide. The entire MR imaging examination took approximately 10 minutes. No patients were ventilator dependent during imaging, and no patients experienced respiratory difficulties.
Pulmonary DSA
All pulmonary angiography examinations were performed by experienced vascular radiologists (J.M.F., A.B.K.) on a DSA system (CAS 8000; Toshiba, Tokyo, Japan) with a 6.3-F Grollman catheter (Cook, Brisbane, Queensland, Australia) or 7-F pigtail catheter (Cordis, Miami, Fla). The maximum rate of each injection of nonionic contrast medium (Omnipaque 300; Nycomed) was 20 mL per second, with a maximum volume of 40 mL per injection. Anteroposterior and posterior oblique projections were obtained routinely, and additional magnified projections were obtained, if necessary, as indicated by the V-P scanning and initial imaging results. The lungs were examined in all cases by using selective right and left pulmonary arterial injections. Pulmonary arterial flow and right heart flow pressures were obtained in all patients. The rate and volume of contrast medium administered was reduced in three patients with pulmonary hypertension, which was defined through local practice as a systolic pulmonary arterial pressure greater than 30 mm Hg or a mean pressure greater than 18 mm Hg.
The angiographers had access to the patients' case notes, chest radiographs, and V-P scanning reports, but they were unaware of the results of MR angiography. All MR angiographic and DSA studies were performed within 24 hours of the V-P scanning.
Interpretation of Images
For both imaging modalities, interpretations were reported on standardized reporting forms. Teigen et al (6) divided the pulmonary arterial tree into 12 vascular zones—that is, seven central zones and five peripheral zones. The central zones were the main pulmonary artery, right and left pulmonary arteries, truncus anterior, right interlobar artery, descending trunk on the left, and left upper lobe trunk. The peripheral zones were the segmental and subsegmental arterial distributions of the right upper lobe, right middle lobe, right lower lobe, left upper lobe, and left lower lobe. Each zone was classified as interpretable or uninterpretable on digital subtraction and MR angiograms.
Each DSA study was interpreted independently by the two radiologists (J.M.F, A.B.K.) who performed the studies. Both of these radiologists are experienced in vascular radiology, and both had the patients' case notes, plain chest radiographs, and V-P scanning reports. If the radiologists' reports differed, then an adjudicator (P.J.D.) made the final decision on the interpretation of the disputed vascular territory, with reference to the reports of both DSA interpreters. Images, with and without subtraction and on film hard copy, were reviewed and manipulated with respect to contrast and brightness on the DSA console. The result of DSA was considered to be the standard method of reference.
MR angiographic studies were interpreted independently by two radiologists experienced in MR imaging (C.K.F., M.J.F.). They had the MR angiogram request forms that contained short clinical histories of the patients, but they had no knowledge of the V-P abnormalities. They were blinded to the case notes and results of chest radiography and DSA. Images were reviewed on a computer workstation (Evaluation Console MRSC; Siemens Medical Systems). Film hard-copy images were obtained for representation but were not used to help make the diagnosis. Raw data images were reviewed and maximum intensity projection (MIP) images were obtained by using overlapping narrow and wide subvolume targeting (Figs 1–3). If the radiologists' reports differed, then an MR adjudicator (S.J.D.) made the final decision on the disputed vascular territory, with reference to the reports of both MR imaging reporters.
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Statistical Analyses
Sensitivity, specificity, and positive and negative predictive values for the detection of acute PE were calculated. For these binomial proportions, the 95% CIs were calculated at the 0.05 level of significance.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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All vascular zones were regarded as interpretable at DSA. Four hundred fifteen of the 432 zones were regarded as interpretable at MR angiography. Seventeen zones were regarded as uninterpretable because of respiratory movement artifact. Thirteen patients had DSA-proved PE, and 23 had normal digital subtraction angiograms. Thirty-four patients had intermediate-probability V-P scans, and two had low-probability scans. All patients with DSA-proved PE had intermediate-probability V-P scans.
Twelve patients had findings positive for emboli at MR pulmonary angiography. Two patients had false-negative MR angiographic findings and one had false-positive findings; this yielded an overall sensitivity of 85% (11 of 13 patients) (95% CI, 64%, 98%) and a specificity of 96% (22 of 23 patients) (95% CI, 85%, 100%) (Table 1). Both cases of false-negative results occurred in patients who had a single small subsegmental embolus. In one patient, the embolus was in the anterior segment of the right upper lobe, and in the second patient, it was in the left lower lobe. These emboli were not visible in retrospect. There was a single false-positive MR angiogram obtained in a patient; the image depicted a small embolus in the right upper lobe peripherally. However, the angiogram was reported as normal by both DSA interpreters. In both false-negative cases, the DSA adjudicator was required owing to disagreement between the two initial interpreters. In the single false-positive case, the MR adjudicator was used.
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Of the six emboli missed by using MR angiography, two were in the right upper lobe, one was in the right lower lobe, one was in the left upper lobe, and two were in the left lower lobe. MR angiography missed two of three right upper lobe emboli and the one left upper lobe embolus. Hence, MR angiography was less accurate at enabling the identification of upper lobe emboli, although two of the four upper lobe emboli were small and subsegmental.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In most centers, V-P scanning is the next most commonly sought examination. Scintigraphic criteria for the likelihood of PE have been modified several times during the past 25 years, and refinements will no doubt continue. Data from the PIOPED study (4) showed that although the sensitivity of this examination is very high (98%), the specificity is very low (10%). The results of scans interpreted as high probability were in agreement with the angiographic diagnosis in 88% of patients, but a minority of patients with DSA-proved PE had a high-probability scan (41%). A substantial proportion of patients with DSA-proved PE had intermediate- (33%) or low-probability (14%) V-P scanning results. This means the majority of patients who have PE will have an inconclusive V-P scanning result.
Clinical signs and symptoms and the results of examinations such as blood tests and electrocardiography have been shown to be unhelpful in establishing the diagnosis in this group of patients (8). Doppler ultrasonography (US) of the legs is often helpful, because the presence of deep venous thrombosis justifies anticoagulation therapy and makes a search for PE unnecessary. However, a normal result does not exclude PE, and even among patients with angiographically proved PE, 50% have positive venous studies of the legs.
In a recent study by Ferretti et al (9), 24.4% of 164 patients with intermediate-probability V-P scans and normal Doppler US scans of the leg had PE that was proved at spiral computed tomography (CT). These results correlate well with those of pulmonary angiography (10) and suggest that rates of a positive Doppler US result in patients with intermediate V-P scans are likely to be very low. The most accurate method of establishing the diagnosis in this group of patients is pulmonary angiography. It allows direct visualization of the pulmonary arterial tree to detect the filling defects that are typical in PE.
There are, however, substantial problems associated with pulmonary angiography. Pulmonary angiography is an invasive procedure in which catheterization of a peripheral vein and manipulation through the tricuspid and pulmonary valves are required. Although the morbidity and mortality associated with this procedure are low and seen almost exclusively in severely ill patients with pulmonary hypertension, many clinicians remain reluctant to request pulmonary angiography because of its invasive nature and prefer instead to make the diagnosis on the basis of clinical findings. Study results (8) show clinical examination findings to be unreliable in patients with intermediate V-P scans and that they probably lead to an incorrect diagnosis in a substantial number of patients.
Although pulmonary angiography is regarded as the standard method of reference, problems in interpreting the images are common. In the PIOPED study (4), although there was good interobserver agreement in the detection of larger emboli, the interobserver agreement decreased to 63% in the detection of small subsegmental emboli. This may be worse with DSA, which is now the most commonly used angiographic technique, because of problems with cardiac pulsation. For this reason, we believe it is important to review images unsubtracted to attempt to reduce cardiac pulsation artifact. At many institutions, including our own, conventional angiography is no longer performed, and DSA has become the standard method by default.
Without anticoagulation therapy, PE has an estimated mortality rate of 30%–36% (11,12), but with anticoagulation therapy, it has a mortality rate of 2.5% (13). However, anticoagulation therapy has complications: The risk of major hemorrhage with therapeutic heparin is 3.4%–7.8%, and with warfarin with an international normalized ratio of 2.0–3.0, the risk is 1.7% (14). Hence, there is a need for accurate diagnosis that is ideally determined noninvasively.
Our study was designed to look at cases that remained diagnostic dilemmas in spite of clinical evaluation and V-P scanning. This probably explains the lack of emboli in the central zones and the preponderance of smaller peripheral emboli in our study, but these findings are a good reflection of those seen in everyday clinical practice and enabled a rigorous test of the described techniques. Also, there were small numbers of emboli in our series compared with the numbers of emboli detected in the study by Remy-Jardin et al (15). In our study, patients with high-probability V-P scans were excluded, and the angiographic criteria for a pulmonary embolus were strict.
In MR pulmonary angiography, one cannot overstress the importance of image review and the comprehensive use of all available techniques of image manipulation. At our institution, each vascular zone is examined in turn, starting with a careful examination of the 42 partitions of raw data. After this, overlapping small, subvolume targeted MIP images are prepared, again with each zone examined in turn. Usually, it is possible to visualize all the abnormalities on the raw data images; however, pulmonary emboli often lodge at a point where there is an abrupt change in vessel caliber, which is most often where the vessel branches, and it may be difficult on single thin coronal sections to tell the difference between a normal bifurcation and a small embolus lying at the bifurcation because only a small part of the component vessels are included in that section (Fig 2c ). It is extremely useful in this situation to obtain MIP images. Small 1–2-cm subvolumes are ideal in this situation, because they produce an image that shows all the components of a branching vessel, which gives the image perspective (Figs 2b, 3). Large subvolumes are less useful because of vessel overlap, but they result in a good overall demonstration of the pulmonary vessels (Fig 2c). Because there is often some degree of unwanted pulmonary venous opacification (Fig 1d), it is useful to obtain larger subvolume MIP images so that vessels can be followed to the hilum to differentiate arteries from veins. A smaller image volume can then be used to concentrate on just the arterial branches. An unwanted superimposed vessel can often be removed by making a small alteration in the size or position of the subvolume.
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The use of correct windowing is important, because it is possible to obscure emboli by using the wrong window setting. It is essential that the reviewing radiologist perform all image manipulations personally rather than delegate this responsibility because of the ease in producing artifact, particularly that due to vessels leaving the image volume. Good results and interobserver agreement can be achieved only when a careful methodical approach to reviewing images is adopted. Although it is easy to learn to use the workstation, image analysis is time-consuming. Even with experience, an average of 20 minutes is required to review each case.
We demonstrated an overall sensitivity of 85% (95% CI, 64%, 98%) and specificity of 96% (95% CI, 85%, 100%). Our results are not as good as those of Meaney et al (16). However, we used half the dose of gadolinium-based contrast media for our study, with a potentially considerable saving in costs. Also, a substantial number of subsegmental emboli were not detected with either angiography or MR imaging in their study; this may have been coincidental or related to their study group but certainly would result in better results with MR imaging. If we had not detected subsegmental emboli, our results would have been similar. Pixel size is a limiting factor in the detection of subsegmental emboli, but this may be overcome with new software developments.
There were two false-negative cases. Both patients were considered at DSA to have small peripheral subsegmental isolated emboli. In both cases, there was disagreement between the DSA interpreters, and the DSA adjudicator was required.
Our results compare favorably with those of recent studies of PE with both CT and MR imaging. Recent developments in spiral and electron-beam CT have improved the depiction of pulmonary arteries and enabled the chest to be imaged in a single breath hold. In several recent articles, the diagnosis of PE with CT has been described. By using spiral CT, Remy-Jardin et al (15) achieved a sensitivity of 100% and a specificity of 96%. However, Goodman et al (17) examined 20 patients by using spiral CT, and although they found good correlation with angiography in the detection of central, lobar, and segmental emboli (sensitivity 85% and specificity 92%), the images demonstrated one of four small subsegmental emboli and thus reduced the overall sensitivity to 63% and the specificity to 89%. They concluded that subsegmental emboli are difficult to diagnose at CT, and therefore pulmonary angiography remains the diagnostic imaging method of choice. Oser et al (18) concluded that if cross-sectional imaging can depict emboli in only segmental and larger branches, then emboli will be missed in 30% of patients.
Teigen et al (6) used electron-beam CT to examine 60 patients suspected of having PE. They reported four false-negative cases due to small peripheral subsegmental emboli. The conclusions they drew were different from those of Goodman et al (17) and Oser et al (18), however, and they assumed small subsegmental emboli to be clinically unimportant in the absence of other demonstrable clots. When these cases were excluded, it brought the sensitivity and specificity of electron-beam CT close to 100%.
Advocates of CT also draw attention to its widespread availability and capability to enable correct diagnosis of pathologic conditions of the chest other than PE to account for the patient's symptoms. The disadvantages of CT include the use of iodinated contrast media and exposure to ionizing radiation.
Several articles in which MR imaging in the diagnosis of PE was investigated have been published recently. These studies have involved the investigation of angiographic and nonangiographic MR imaging techniques. In several studies, pulmonary emboli have been demonstrated on spin-echo images (19–23); however, slow blood flow may mimic emboli by producing identical high-signal-intensity foci. A variety of pulse sequences have been used with varying success to try to overcome this problem (24–28).
Other major problems with pulmonary MR angiography include cardiac and respiratory movement artifact, complex blood flow patterns, and magnetic susceptibility effects from air-containing lungs. Advances in MR imaging technology have, however, led to the recent development of single-breath-hold three-dimensional gradient-recalled-echo sequences. When these are combined with gadolinium enhancement, excellent angiographic images are produced. In a recent study, Meaney et al (16) used such a sequence with gadolinium enhancement and quoted an overall sensitivity of 100% and a specificity of 95%.
It seems clear from recent literature that both MR imaging and CT are highly accurate in demonstrating lobar and segmental emboli with MR angiography. Neither examination, however, has to date been particularly successful in demonstrating small peripheral subsegmental emboli. In our study, we were able to identify one of five subsegmental emboli with MR angiography. There is much controversy regarding the importance of subsegmental emboli. One view is that small subsegmental emboli arise from isolated calf vein thrombi, are not important, and may require no treatment (29,30). Others believe that these may be the harbinger of larger life-threatening emboli and therefore require treatment. A substantial number of patients may have only isolated subsegmental emboli: In our series, 15.4% (two of 13) patients had isolated subsegmental emboli, but others have quoted up to 30% (18).
If patients with small subsegmental emboli were regarded as having clinically important disease for which they do not require treatment, then the literature would support the replacement of pulmonary angiography—and possibly V-P screening—with CT or MR imaging, depending on local expertise and availability. However, if such patients really need anticoagulation therapy, then the literature would suggest the possibility of an underdiagnosis by using MR imaging only or CT only in up to one-third of cases. One potential safeguard would be to include an assessment of clot burden in these patients, and the routine addition of Doppler US in algorithms with CT or MR imaging has been suggested (31). Although the majority of pulmonary emboli originate in the lower limbs (10,32), clinically important emboli can arise in the pelvic veins, inferior vena cava, and renal veins. With the increased use of central lines, an increasing number of emboli are described as arising from the subclavian and brachiocephalic veins (33,34). Lower-limb venous studies are positive in half the patients with proved pulmonary emboli (35).
Improvements in MR angiographic techniques will inevitably produce better results in the future. The ability to time the sequences so that images can be obtained during the peak of pulmonary arterial opacification is desirable. Such a timing sequence has recently been described by Prince et al (36) and has recently become commercially available. Faster imaging techniques with short TRs and TEs will lead to shorter breath holds, less movement artifacts, and improved resolution. Cardiac gating and subtraction techniques will be used more reliably. Finally, blood pool vascular contrast media for MR imaging are already being developed and offer much promise in this field.
In summary, gadolinium-enhanced MR angiography is an excellent noninvasive technique for imaging the pulmonary arteries and is very accurate in depicting central, lobar, and segmental emboli, but at this stage, it is unreliable in depicting small subsegmental emboli.
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Acknowledgments |
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Footnotes |
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Address reprint requests to C.K.F.
See also the editorial by Yucel (pp 301–303) in this issue.
Abbreviations: DSA = digital subtraction angiography MIP = maximum intensity projection PE = pulmonary embolism V-P = ventilation-perfusion
Author contributions: Guarantor of integrity of entire study, L.A.C.; study concepts and design, C.K.F., J.M.F., S.J.D.; definition of intellectual content, C.K.F., A.G., J.M.F.; literature research, A.G., C.K.F.; clinical studies, A.G., C.K.F., A.B.K., J.M.F., M.J.F., I.T.M., P.J.D.; data acquisition, C.K.F., A.B.K., J.M.F., M.J.F., I.T.M, P.J.D.; data analysis, A.G., C.K.F., L.A.C.; statistical analysis, A.G.; manuscript preparation, A.G., C.K.F.; manuscript editing, C.K.F., M.J.F., S.J.D.; manuscript review, A.G., C.K.F., M.J.F., S.J.D., L.A.C.
Received February 24, 1998;
revision requested May 5, 1998; revision received June 12, 1998;
accepted August 10, 1998.
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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R. C. Gaba, R. C. Carlos, W. J. Weadock, G. P. Reddy, M. B. Sneider, and P. N. Cascade Cardiovascular MR Imaging: Technique Optimization and Detection of Disease in Clinical Practice RadioGraphics, November 1, 2002; 22(6): e6 - e6. [Abstract] [Full Text]
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R.-C. Chen, W.-T. Chen, H.-Y. Tu, N.-Y. Cheng, C.-K. Wang, L.-Y. Liao, C.-S. Wang, and P.-H. Chen Assessment of Vascularity in Hepatic Tumors: Comparison of Power Doppler Sonography and Intraarterial CO2-Enhanced Sonography Am. J. Roentgenol., January 1, 2002; 178(1): 67 - 73. [Abstract] [Full Text] [PDF]
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N.L. Muller Advances in imaging Eur. Respir. J., November 1, 2001; 18(5): 867 - 871. [Abstract] [Full Text] [PDF]
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S. Kruger, P. Haage, R. Hoffmann, C. Breuer, A. Bucker, P. Hanrath, and R. W. Gunther Diagnosis of Pulmonary Arterial Hypertension and Pulmonary Embolism With Magnetic Resonance Angiography Chest, November 1, 2001; 120(5): 1556 - 1561. [Abstract] [Full Text] [PDF]
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P. S. Wells, D. R. Anderson, M. Rodger, I. Stiell, J. F. Dreyer, D. Barnes, M. Forgie, G. Kovacs, J. Ward, and M. J. Kovacs Excluding Pulmonary Embolism at the Bedside without Diagnostic Imaging: Management of Patients with Suspected Pulmonary Embolism Presenting to the Emergency Department by Using a Simple Clinical Model and D-dimer Ann Intern Med, July 17, 2001; 135(2): 98 - 107. [Abstract] [Full Text] [PDF]
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T. P. Smith Pulmonary Embolism: What's Wrong with This Diagnosis? Am. J. Roentgenol., June 1, 2000; 174(6): 1489 - 1497. [Full Text]
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D. D. Maki, W. B. Gefter, and A. Alavi Recent Advances in Pulmonary Imaging Chest, November 1, 1999; 116(5): 1388 - 1402. [Abstract] [Full Text] [PDF]
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M. Goyen, A. Gupta, and C. K. Frazer CT reinterpretation. Radiology, August 1, 1999; 212(2): 601 - 602. [Full Text]
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E. K. Yucel Pulmonary MR Angiography: Is It Ready Now? Radiology, February 1, 1999; 210(2): 301 - 303. [Full Text]
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