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1 All authors: Department of Radiology, West Virginia University, School of Medicine, Robert C. Byrd Health Sciences Center, P. O. Box 9235, Morgantown, WV 26505-9235.
Received February 13, 2002;
accepted after revision April 26, 2002.
Address correspondence to D. R. Martin.
Abstract
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SUBJECTS AND METHODS. Paired gadolinium-enhanced 2D gradient-echo and 3D gradient-echo VIB images were acquired in 15 consecutive patients with suspected intrathoracic abnormalities. MDCT scans were available for comparison in 12 patients. Two reviewers independently analyzed the MR images obtained using the two techniques for overall quality, the degree of artifacts, and visibility of mediastinal or parenchymal abnormalities. The detectability of lesions on the 3D gradient-echo VIB images and 2D gradient-echo images was compared with the detectability of lesions on CT scans obtained in nine patients.
RESULTS. In all cases, the MR images obtained using the 3D
gradient-echo technique with the VIB sequence were rated superior to those
obtained using the 2D gradient-echo technique for quality, depiction of
mediastinal structures, and clarity of pulmonary vessels and central airways.
On the 3D gradient-echo VIB images, the degree of phase artifacts was lower
(p < 0.001), but the degree of pixel graininess was higher
(p < 0.05). Detectability, confidence and conspicuity levels, and
marginal delineation of the pulmonary lesions were rated higher statistically
on the 3D gradient-echo VIB images than on the 2D gradient-echo images. Of the
31 solid pulmonary abnormalities depicted on MDCT, 27 (87.1%) were detected on
the 3D gradient-echo VIB images, and 21 (67.7%) were seen on the 2D
gradient-echo images (p < 0.05). The 3D gradient-echo VIB images
showed all 14 mediastinal lesions (100%) seen on MDCT, whereas the 2D
gradient-echo images showed 12 (85.7%) of the 14 lesions (p 
0.05).
CONCLUSION. The gadolinium-enhanced modified 3D gradient-echo technique with the VIB sequence provides MR images that are superior in quality, have significantly fewer artifacts, and have a higher sensitivity for the detection of intrathoracic lesions compared with images obtained using the standard 2D gradient-echo technique.
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A recently introduced modified three-dimensional (3D) gradient-echo technique with a volumetric interpolation during breath-hold (VIB) sequence holds promise for overcoming the effects of motion artifacts and provides improved quality images of normal and diseased lung parenchyma during a single breath-hold [8, 9]. This MR technique allows the generation of volumetric T1-weighted high-resolution images of the soft tissues during a single breath-hold with near-isotropic voxels on the order of 2.5 mm [10, 11]. Few reports describe fast 3D gradient-echo VIB imaging of the soft tissues, but the results in imaging the liver are encouraging [10,11,12,13]. Recently, the 3D gradient-echo VIB technique was found to be superior to the 2D gradient-echo technique with regard to MR image quality in showing the lungs of healthy volunteers [8] and to be useful in evaluating patients with benign and malignant lung diseases [9]. Nevertheless, experience with modified 3D gradient-echo VIB imaging of the chest has been limited, and a relative comparison with multidetector CT (MDCT) scans of patients with intrathoracic abnormalities has not, to our knowledge, been reported. CT is the current gold standard for cross-sectional imaging of the lungs.
The purpose of our study was to assess the clinical feasibility of MR imaging of the thorax, including the lungs, using a gadolinium-enhanced fat-suppressed modified 3D technique with a VIB sequence compared with using a standard 2D gradient-echo technique or MDCT. Image quality, degree of artifacts, delineation of parenchymal and mediastinal vessels and airways, and detectability of focal parenchymal or mediastinal lesions were evaluated and compared for all images.
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MDCT scans were available in 12 patients. MDCT was performed within a median time interval of 62 days (range, 0-201 days) before or after MR imaging. Three patients (two with benign indications and one with an extrathoracic malignancy) were excluded from the MDCT—MR imaging comparison because the interval between the MDCT and MR examinations was too long, between 83 and 201 days, thus increasing the potential for lesions to change in size and number. In the remaining nine patients with MDCT scans, MDCT and MR examinations were performed within 1 week in four patients, within 1 month in four patients, and within 3 months in one patient. The interval between MDCT and MR examinations was less than 18 days in all seven patients with primary or secondary lung cancer.
Image Acquisition
MR imaging.—All chest MR imaging and MDCT examinations were
performed during suspended full inspiration. MR imaging was performed on a
1.5-T superconducting system (Symphony with Quantum gradients; Siemens Medical
Systems, Iselin, NJ) using phased array surface anterior and posterior coils.
In all cases, after unenhanced T1- and T2-weighted MR images were obtained,
gadolinium-enhanced 2D gradient-echo (fast low-angle shot) and modified 3D
gradient-echo VIB images were obtained in the axial plane within 60-70 sec
after starting IV administration of 0.1 mmol/kg of gadopentetate dimeglumine
(Magnevist; Berlex Laboratories, Wayne, NJ) at a rate of 2 mL/sec followed by
a 20-mL saline flush through an antecubital vein using a power injector. In
all patients, 3D gradient-echo VIB images were acquired first, immediately
followed by 2D gradient-echo imaging. Fat-suppression was applied to both the
2D gradient-echo and the 3D gradient-echo VIB sequences. The field of view was
380 mm with a rectangular configuration in the phase-encoding direction and
was kept constant for all sequences.
The MR imaging parameters for the 3D gradient-echo VIB sequence were as follows: TR/TE, 3.7/1.7; flip angle, 150°; acquisition matrix, 176 x 256; section thickness, 2.5 mm; and receiver bandwidth, 260 Hz/pixel. The slab thickness was 300 mm divided into 120 partitions with a partition thickness of 2.5 mm. The whole set of images was obtained during a single breath-hold.
The MR imaging parameters for the 2D gradient-echo sequence were as follows: 149/5.2; flip angle, 700°; acquisition matrix, 176 x 256; section thickness, 5 mm with 15% interslice gap; and receiver bandwidth, 260 Hz/pixel. Images were acquired during two contiguous breath-hold periods of 26 sec each with a 2-cm overlap between acquisition slabs to cover the entire chest.
MDCT.—All chest CT examinations were performed with a four-row MDCT scanner (Light-Speed QX/i; General Electric Medical Systems, Milwaukee, WI) during a single breath-hold, typically requiring between 20 and 25 sec, using 200-400 mA, 120 kV, a 5-mm collimation with a 2.5-mm reconstruction, and a 10-mm table feed per rotation. The field of view was 360 x 360 mm with an acquisition matrix of 512 x 512. In 10 patients, MDCT scans were obtained after the IV infusion of 140 mL of 300 mg I/mL of iohexol (Omnipaque 300; Nycomed, Princeton, NJ) through an antecubital vein at a rate of 3 mL/sec using a power injector. Two patients underwent unenhanced MDCT because kidney function was poor.
Image Analysis and Statistics
MR images were reviewed on a computer workstation (PathSpeed version 8.1;
General Electric Medical Systems). Two radiologists independently analyzed the
axial gadolinium-enhanced 2D gradient-echo and 3D gradient-echo VIB images
without knowing the MDCT findings.
The reviewers subjectively assessed image quality (overall clarity of both central lung anterior and posterior to the mediastinum, and peripheral lung) and the level of depiction of central and peripheral pulmonary vessels, mediastinal structures (heart, great vessels, azygos vein, and esophagus), and central airways to the level of segmental bronchi. For each of these assessments, the reviewers provided a numeric score from 1 to 4, representing nondiagnostic (uninterpretable), poor, fair, and good, respectively. The degree of image degradation due to pulsation, patient motion, and pixel graininess was also assessed using a scale of from 1 to 4, indicating severe, moderate, mild, or negligible, respectively. When a parenchymal or mediastinal lesion was detected, each reviewer independently recorded the presence and location of the lesion and assessed lesion conspicuity and delineation of margins using a scale of from 1 to 4, indicating nondiagnostic, poor, fair, and good, respectively. The reviewers also assigned a confidence level to each abnormality they observed using a grading scale. A score of 1 was designated if a reviewer did not detect a lesion, and scores ranging from 2 to 4 indicated uncertain, probable, or definite, respectively. Any rounded or ovoid lesion in the lung parenchyma measuring less than 3 cm was defined as a lung nodule, whereas a similar lesion 3 cm or larger was regarded as a mass. In cases of discrepancies between reviewers regarding lesion detection, a final interpretation was obtained by consensus during a second session. Lesion size was determined by electronic measurement on the workstation monitor, and decimals were rounded to the nearest millimeter.
After MR imaging analysis was completed, MDCT images were used as a gold standard for determining the presence of an intrathoracic abnormality. Each study was reviewed using a side-by-side comparison of the MDCT and MR images during a consensus review session. The detectability of lesions on the 2D gradient-echo and 3D gradient-echo VIB images was compared with the detectability of lesions on MDCT scans using a lesion-by-lesion analysis in nine of 12 patients who underwent both MDCT and MR imaging examinations. Three patients who underwent MDCT were excluded from the comparison because the interval between MDCT and MR examinations was excessive.
Statistical analysis was performed with version 10.0 of the Statistical Package for the Social Sciences computer program (SPSS, Chicago, IL). Wilcoxon's signed rank test was used to assess the statistical significance of the differences between the scores for image quality, degree of artifacts, subjective confidence, and lesion conspicuity for the 2D gradient-echo images versus those for the 3D gradient-echo VIB images in the same patients using the mean of the scores of the two reviewers. For the purpose of rank testing, the lesions with a confidence level of either 3 or 4 were considered as confidently detected, whereas the lesions with a confidence level of either 1 or 2 were considered undetected. The McNemar test was used to evaluate for statistical differences in lesion detection, with p values of less than 0.05 indicating a statistically significant difference.
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0.05) was found between the scores of
the two reviewers with regard to image quality; depiction of the central
pulmonary vessels, mediastinal structures, and central airways; and degree of
image artifacts. The interobserver agreement in the evaluation of image
quality was moderate for the 3D gradient-echo VIB images (
= 0.47) and
fair for the 2D gradient-echo images ( = 0.25). The two reviewers
showed agreement in grading none of the 2D gradient-echo images as good for
quality. The average assessment for the 2D gradient-echo images was fair,
whereas the quality of the 3D gradient-echo VIB images was graded as good on
average (Table 1). Variation
between the two reviewers' scores occurred when rating the image quality as
poor or fair for the 2D gradient-echo images (n = 4) and as fair or
good for the 3D gradient-echo VIB images (n = 3).
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In all cases in our study, the scores for image quality, visualization of
mediastinal structures, clarity of central and peripheral pulmonary vessels,
and depiction of central airways on the images obtained were higher for the 3D
gradient-echo VIB images than for the 2D gradient-echo images; these
differences achieved statistical significance
(Table 1). All 3D gradient-echo
VIB images were of fair or good quality for the evaluation of the central and
peripheral lung (Figs.
1A,1B,1C,2A,2B,2C,3A,3B,3C,4A,4B,4C,5A,5B,5C).
The degree of phase artifacts from pulsation was statistically lower on the 3D
gradient-echo VIB images than on the 2D gradient-echo images (p <
0.001) (Figs.
1A,1B,1C
and
2A,2B,2C).
Phase artifacts caused a pseudolesion on 2D gradient-echo images (Fig.
3A,3B,3C).
The degree of image graininess, however, was significantly higher on the 3D
gradient-echo VIB images than on the 2D gradient-echo images (p <
0.005). Image artifacts due to patient motion did not differ statistically
between the two MR techniques (p 0.05).
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Lesion Detection
Two-dimensional gradient-echo versus 3D gradient-echo
VIB.—Of 15 patients, two had normal findings on MR examinations. In
13 patients, 3D gradient-echo VIB images showed 31 lung abnormalities (two
pulmonary masses [two squamous cell carcinomas, 32 x 20 mm and 35
x 31 mm], 24 pulmonary nodules [range, 3-18 mm; mean, 8 mm], and five
areas of fibrosis or atelectasis) and 14 mediastinal lesions (one mediastinal
mass [thyroid cyst, 65 x 60 mm] and 13 mediastinal or hilar lymph nodes
[range, 8-28 mm; mean, 16 mm]). The 2D gradient-echo images showed 24 lung
abnormalities (one pulmonary mass, 20 pulmonary nodules, and three areas of
fibrosis or atelectasis) and 12 mediastinal lesions (one mediastinal mass and
11 mediastinal or hilar lymph nodes). The pulmonary mass, two pulmonary
nodules, and two lymph nodes that were overlooked on 2D gradient-echo images
were reassessed retrospectively and found to be poorly visible, but the
confidence level for detection was insufficient to classify the lesions as
focal lesions (Fig.
4A,4B,4C).
Intrathoracic lesion conspicuity was ranked as fair for six lesions (19.4%) and as good for 25 lesions (80.7%) on 3D gradient-echo VIB images. Scores for lesion detectability, confidence and conspicuity levels, marginal delineation of pulmonary lesions, and conspicuity of mediastinal lesions were statistically higher for the 3D gradient-echo VIB images than for the 2D gradient-echo images (Table 2 and Figs. 2A,2B,2C and 4A,4B,4C).
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MR imaging versus MDCT.—MDCT scans were available for 12 of
the 15 patients, but three patients were excluded because the period between
the MDCT and MR imaging examinations was too long. In the remaining nine
patients, 3D gradient-echo VIB images showed all 14 mediastinal lesions (100%)
and 27 (87.1%) of the 31 solid lung abnormalities seen on MDCT, whereas 2D
gradient-echo images detected 12 (85.7%) of the 14 mediastinal lesions and 21
(67.7%) of the 31 solid pulmonary lesions. The difference between the 2D
gradient-echo images and the 3D gradient-echo VIB images for the detection of
solid lung abnormalities was significant (p < 0.05). However, when
areas of fibrosis or atelectasis were ignored, the difference between the two
MR techniques in the detection of pulmonary masses and nodules was not
significant (p 0.05).
Of two lung masses and five areas of fibrosis or atelectasis seen on MDCT,
all were detected on 3D gradient-echo VIB images, but only one lung mass and
three areas of fibrosis or atelectasis were seen on 2D gradient-echo images.
Of the 24 pulmonary nodules seen on MDCT (range, 3-18 mm; mean, 8 mm), 20
lesions (83.3%) were detected on the 3D gradient-echo VIB images, and 17
(70.8%) were seen on the 2D gradient-echo images (Figs.
1A,1B,1C
and
4A,4B,4C).
The detection of nodules according to size is presented in
Table 3. Differences between
the two MR techniques in the scores for detectability of lung nodules and
confidence level were not significant (p 0.05), but the scores
for lesion conspicuity and marginal delineation were significantly higher for
the 3D gradient-echo VIB images than for the 2D gradient-echo images
(p < 0.05). All the nodules that were missed on 3D gradient-echo
VIB images were 5 mm or smaller in diameter, and three of the four overlooked
nodules were visible at a retrospective lesion-by-lesion analysis (Fig.
5A,5B,5C).
One lesion undetected even on retrospective assessment was a calcified nodule
measuring 5 mm. Four of the seven nodules that were missed on 2D gradient-echo
images were smaller than 5 mm, but three ranged between 6 and 10 mm. In no
case did 2D gradient-echo images show a nodule that was not depicted on 3D
gradient-echo VIB images. Three of the seven initially overlooked nodules were
also detectable on 2D gradient-echo images at retrospective analysis.
Emphysematous changes seen in three patients on MDCT were not visible on MR
images, although severe changes in one patient were visible in retrospect on
3D gradient-echo VIB images.
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The main advantages of the 3D gradient-echo technique with a VIB sequence are its ability to rapidly acquire a volumetric data set during a single breath-hold, which enables acquisition of contiguous thin-slice images with no interslice gap, and its ability to allow dynamic imaging after gadolinium administration. Moreover, because the 3D technique is relatively insensitive to phase artifacts, the depiction of lesions is improved. In contrast to the excitation volume for the 2D MR technique, the excitation volume for the 3D MR technique is phase-encoded in two independent directions, perpendicular (phase-encoding) and parallel (section- or partitions-encoding) to the plane of excitation. Asymmetric sampling performed in each of the phase-encoding directions improves spatial resolution [10, 11]. When coupled with zero-filling interpolation, smaller pixels can be generated without prolonging imaging times.
The administration of gadolinium in this study might have contributed to the increased contrast-to-noise ratio and lesion conspicuity, although the benefit of gadolinium enhancement was not specifically tested in this study. The 3D gradient-echo VIB images also enabled superior evaluation of the mediastinum and superior delineation of the heart borders with decreased scanning time as compared with 2D gradient-echo images. The reduction in image artifacts is another factor that improved image quality in our study. The 3D gradient-echo VIB technique has a shorter TE that minimizes signal loss from susceptibility dephasing due to the short T2* relaxation time (5-10 msec) of aerated lung parenchyma [14]. On standard 2D gradient-echo images, phase artifacts from cardiac and respiratory motion deteriorated image quality in the central lung and mediastinum interfering with lesion detection and causing a pseudolesion. Cardiac gating would have improved the quality of the 2D gradient-echo images, but acquiring a good cardiac gate in patients with arrhythmia may be difficult. We did not use cardiac gating in this study to show how cardiac motion affected the quality of the 2D gradient-echo and 3D gradient-echo VIB images.
In this study, the 3D gradient-echo VIB images were affected by negligible pulsation artifacts compared with 2D gradient-echo images and thus more clearly depicted the central lung, mediastinal structures, and airways. Phase artifacts due to cardiac pulsation not only mimicked the appearance of a cavitary lesion in one case, but also obscured focal abnormalities such as pulmonary nodules or masses. The lesser degree of phase artifacts on 3D gradient-echo VIB images can be, at least partly, explained by the shorter TE and two phase-encoding directions, which may blur artifacts across the image in two directions so that artifacts become less apparent. On 2D gradient-echo images, phase-related artifacts resulted in a series of parallel lines across the phase direction (Figs. 1A,1B,1C and 2A,2B,2C). Because the most critical time of image contrast data collection (center of k-space) is significantly reduced for the 3D gradient-echo VIB technique because of implementation of centric-ordered k-space as opposed to linear ordering used for the 2D gradient-echo technique, artifacts causing signal misregistration may be less pronounced on 3D gradient-echo VIB images [15]. Suppression of fat on either MR technique may also contribute to image quality by decreasing motion artifacts from otherwise high-signal subcutaneous and mediastinal fat. The 3D gradient-echo VIB images appeared grainier than the 2D gradient-echo images because the signal-to-noise ratio for the 3D gradient-echo VIB images was diminished by the shorter TR, smaller flip angle, and thinner slice reconstruction.
To our knowledge, only two reports about the usefulness of 3D fast gradient-echo acquisition for chest imaging have been published [8, 9]. The results from these studies were in agreement with our findings, which showed that improved quality and negligible artifacts allow solid or nonsolid pulmonary diseases to be depicted on gadolinium-enhanced 3D gradient-echo VIB images with higher lesion conspicuity. However, in the previous studies, a CT comparison was not performed and fat suppression was not applied.
This study is the first to assess the feasibility of imaging the lungs using a 3D gradient-echo MR technique with a VIB sequence compared with MDCT. We found that the gadolinium-enhanced MR images obtained using the fat-suppressed 3D gradient-echo technique and the VIB sequence were comparable to MDCT scans for the detection of solid pulmonary and solid or cystic mediastinal lesions. Fat suppression was thought to improve visualization of the mediastinum, chest wall, and axilla for both techniques and was critical for the detection of mediastinal nodes, which were seen as a focus of high signal intensity on the darkened background of suppressed fat. Scores for conspicuity and marginal delineation of lesions and subjective confidence levels were also higher for the 3D gradient-echo VIB images than the 2D gradient-echo images. Fewer lesions were detected on 2D gradient-echo images, and the confidence levels were lower for the abnormalities that were detected. The higher scores for confidence in lesion detection and conspicuity of lesions for the 3D gradient-echo VIB images can be explained by the minimized partial volume effects due to thinner slices and by the improved image quality due to a lesser degree of motion and pulsation artifacts.
Similar to helical volumetric CT, the 3D gradient-echo VIB technique allows continuous data acquisition during a single breath-hold. This capability reduces the chance of a nodule being undetected because of respiratory motion or partial volume averaging and minimizes the risk of a vessel being labeled as a nodule. On the contrary, 2D gradient-echo sequences require use of relatively thicker slices with interslice gaps, which may cause subcentimeter nodules to be missed or poorly characterized as a result of partial volume averaging. In this study, the sensitivity of 3D gradient-echo VIB imaging for depicting nodules was 83% compared with 71% for 2D gradient-echo imaging. The 3D gradient-echo VIB technique detected more pulmonary nodules, with 100% sensitivity for nodules larger than 5 mm in diameter, whereas three nodules measuring 6-10 mm and one mass measuring greater than 3 cm were missed on 2D gradient-echo imaging. On retrospective examination, all nodules missed on 3D gradient-echo VIB images could be identified except one calcified nodule that was seen on MDCT images. Our results are comparable to those previously reported, which showed 84% sensitivity using turbo spin-echo sequences [1] and 82% sensitivity using the STIR technique [2]. However, in contrast to the results of previous studies, our findings revealed that no nodule larger than 5 mm was missed on 3D gradient-echo VIB images. Therefore, if pulmonary nodules smaller than or equal to 5 mm are excluded, the sensitivity of 3D gradient-echo VIB imaging increases to 100% in this study, which is higher than previous reports of 91.8% sensitivity of turbo spin-echo sequences for nodules greater than 5 mm [1] and 92% sensitivity of the STIR technique for nodules larger than 10 mm [2]. Furthermore, the acquisition time was much shorter with the 3D gradient-echo VIB technique. All nodules that were missed on 3D gradient-echo VIB images in this study were 5 mm or smaller, and most—three of four—were visible in retrospective analysis. Although CT has been regarded as a standard reference technique for detection of pulmonary nodules, it is associated with a relatively high level of ionizing radiation—from 10 to 100 times more than chest radiography [16]. Currently, MR imaging cannot replace CT in the evaluation of pulmonary nodules. However, the 3D gradient-echo VIB technique appears to hold promise in the detection of nodules, and familiarity with this technique will likely increase its sensitivity. Nevertheless, the number of patients and nodules in this study is not enough to draw a definite conclusion. The potential for improved detection, delineation, or localization of intrathoracic masses on 3D gradient-echo VIB images using multiplanar reconstruction was also not tested in this study, but has been shown to be helpful in the detection of liver lesions [10, 11]. Additional studies with large numbers of pulmonary nodules are necessary to determine the reliability and reproducibility of this technique before it can be substituted for CT. This MR technique may be particularly useful in patients who would otherwise be exposed to a substantial cumulative dose of radiation from undergoing repeated chest CT, such as in young patients requiring repeated imaging for nonspecific pulmonary nodules or in patients with known pulmonary metastases undergoing tumor therapy.
One of the shortcomings of MR imaging in the evaluation of nodules is its insensitivity to calcification because of the short T2 relaxation time and fewer protons in calcified tissue. We found one example of this shortcoming: a 5-mm calcified nodule that was inconspicuous and similar to the low-signal-intensity back-ground of pulmonary parenchyma was not detected on MR imaging. Similarly, MR imaging may have diminished sensitivity for detection of calcified metastases.
Our study has several limitations. First, our study population was small. However, our intent was to show the feasibility of using the 3D gradient-echo technique with the VIB sequence for chest MR imaging, and the results provided statistically significant differences in image quality and lesion detection. Second, the slice thickness used for the two MR techniques tested was not the same. We acquired 2.5-mm slices with the 3D gradient-echo VIB technique to match the thickness of the MDCT slices. Two-dimensional gradient-echo images were set to 5 mm as a compromise between the desire to produce thin slices and the need to acquire images covering the entire chest during a breath-hold. A postprocessing reconstruction of 3D gradient-echo VIB images with thicker slices could have been performed, but it was thought to be outside the scope of our feasibility study. Third, we did not compare the enhanced images with unenhanced images because no logical benefit to unenhanced examinations could be hypothesized. Further-more, the time delay for the initiation of imaging after gadolinium administration was based on the desire to obtain images during the equilibrium phase of enhancement to minimize the differences between two techniques acquired at different times.
In conclusion, using a gadolinium-enhanced modified 3D gradient-echo technique with a VIB sequence has potential clinical utility for the MR evaluation of the chest. This MR technique significantly reduces artifacts and better depicts abnormalities and could replace the 2D gradient-echo technique for chest MR examinations. The routine use of volumetric 3D gradient-echo VIB imaging would likely make MR imaging serve as an alternative test, particularly if minimizing exposure to ionizing radiation or avoiding the use of iodinated contrast material represents an important clinical concern. Additional studies are warranted to establish the clinical value of this MR technique in patients with various chest diseases.
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