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Gastrointestinal Imaging |
1 From the Department of Radiology, Thomas Jefferson University Hospital, 132 S 10th St, 1096 Main Bldg, Philadelphia, PA 19107. Received May 10, 2000; revision requested June 18; final revision received November 17; accepted December 5. Address correspondence to D.G.M. (e-mail: donald.mitchell@mail.tju.edu).
| ABSTRACT |
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MATERIALS AND METHODS: In 21 patients with focal hepatic lesions, identical T2-weighted breath-hold fast spin-echo images were obtained before and after gadolinium enhancement and were compared regarding lesion-to-liver contrast-to-noise ratio, signal-to-noise ratio, lesion conspicuity, and vascular pulsation artifact. Image review was performed independently, in random order, by two experienced radiologists.
RESULTS: For solid lesions, the lesion-to-liver contrast-to-noise ratio on enhanced images was significantly higher (P < .05) than that on nonenhanced images. For nonsolid lesions, however, there was no significant difference (P = .07). For both readers, lesion conspicuity for solid lesions on enhanced images was significantly higher than on nonenhanced images (P < .05). Severity of vascular pulsation artifact was not significantly different.
CONCLUSION: Solid-lesion contrast on T2-weighted breath-hold fast spin-echo images improves after administration of a gadolinium chelate. These images should be obtained after, rather than before, gadolinium enhancement.
Index terms: Gadolinium Liver, MR, 761.121411, 761.121412, 761.12143 Liver neoplasms, diagnosis, 761.312, 761.319, 761.323 Magnetic resonance (MR), contrast enhancement, 761.12143
| INTRODUCTION |
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In tissues with a substantial concentration of paramagnetic ions from an administered contrast agent, recovery from MT saturation is more rapid, reducing MT-induced signal intensity loss (15,16). In addition, enhancement on T1-weighted images would produce higher signal intensity from stimulated echoes. We hypothesized that solid lesions in liver, by virtue of a larger interstitial space and generally greater enhancement compared with liver on delayed gadolinium-enhanced images, may have improved contrast on T2-weighted breath-hold fast SE images obtained after administration of a gadolinium chelate. The purpose of our study was to test this hypothesis.
| MATERIALS AND METHODS |
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Eight patients had hepatocellular carcinoma, seven had metastasis (colon, n = 2; lung, pancreas, stomach, adrenal gland, and melanoma, n = 1 each), five had cavernous hemangioma, two had a simple cyst, and one had focal nodular hyperplasia. Two patients had two different lesions (one patient had four metastases and one hemangioma, and one had one hepatocellular carcinoma and one hemangioma). Two patients had two different lesions, which were evaluated separately for our quantitative and qualitative analysis. There were a total of 21 hepatocellular carcinomas, 26 metastases (colon, n = 9; lung, n = 1; pancreas, n = 2; stomach, n = 7; adrenal gland, n = 4; melanoma, n = 3), seven hemangiomas, three cysts, and one focal nodular hyperplasia.
For image analysis, metastasis, hepatocellular carcinoma, and focal nodular hyperplasia were classified as solid lesions, and hemangioma and cyst were classified as nonsolid lesions. The largest transverse diameter of the solid lesions ranged from 0.7 to 8.0 cm (mean, 3.1 cm). The largest transverse diameter of the nonsolid lesions ranged from 0.5 to 10.0 cm (mean, 2.7 cm).
Proof of hepatocellular carcinoma was obtained at percutaneous liver biopsy in five patients, two of whom had nine additional hepatocellular carcinomas that were not examined at biopsy. In the other three patients with six hepatocellular carcinomas, proof was based on increased
-fetoprotein levels and progression at follow-up MR examination. Hepatic metastases were diagnosed at biopsy in four patients who had a total of 14 additional lesions that were not examined at biopsy. In the other three patients with six metastases, diagnosis was based on lesion progression at serial MR or computed tomographic (CT) examinations. In patients with multiple malignant lesions, only one lesion was proved malignant at biopsy; in the other lesions, malignancy was presumed on the basis of a similar imaging appearance and/or growth at subsequent examinations. Focal nodular hyperplasia was confirmed at biopsy. Cavernous hemangioma and cyst were diagnosed on the basis of progressive nodular enhancement at dynamic gadolinium-enhanced MR imaging, a hyperintense appearance on heavily T2-weighted MR images, nodular enhancement at CT, or a hyperechoic appearance with increased sound transmission at ultrasonography (17).
MR Imaging
MR studies were performed with a 1.5-T superconducting system (Signa; GE Medical Systems, Milwaukee, Wis) by using a phased-array torso coil. All patients underwent an identical breath-hold T2-weighted fast SE sequence before and about 5 minutes after intravenous bolus administration of 20 mL of gadopentetate dimeglumine (Magnevist; Berlex, Wayne, NJ). In all cases, the contrast agent was administered for dynamic multiphasic gradient-echo imaging, as per our standard clinical protocol for liver imaging. Imaging parameters were 2,000 2,600/8088 (repetition time msec/effective echo time msec); echo train length, 16; bandwidth, ±62 kHz; excitation flip angle, 90°; matrix size, 256 x 128; section thickness, 7 mm; intersection gap, 0.5 mm; rectangular field of view, 32 x 24 cm; and one signal acquired. Twelve sections were simultaneously obtained in one breath-hold; two overlapping stacks of 12 sections were obtained to image the whole liver. Gradient moment nulling in the section-select axis and saturation bands superior and inferior to the imaging volume were used to reduce the severity of flow-related artifacts. Fat signal was suppressed by the addition of frequency-selective fat-saturation pulses.
Image Analysis
For qualitative analysis, hard copies of each image set were reviewed by two experienced radiologists (D.G.M., G.A.H.). To minimize learning bias, patient data and imaging parameters were removed from the images, and both image sets were reviewed independently and in random order. There were two reading sessions separated by 4 weeks. Each session included half the images from the nonenhanced and gadolinium-enhanced groups mixed randomly. Lesion conspicuity was rated according to a four-point scale: 1, poor; 2, moderate; 3, good; and 4, excellent. Presence of vascular pulsation artifact was graded with a four-point scale: 1, severe; 2, moderate; 3, mild; and 4, minimum. The subset of patients with solid lesions was further examined separately. For each session, the readers recorded the size and site (Couinaud segment) of visible lesions. Only lesions that were identified by both readers were included for analysis. There was no difference in the number of missed lesions for both readers. Multiple lesions of the same type in a given patient were averaged for qualitative analysis so that there was one measure of lesion conspicuity for this patient on each image.
For quantitative analysis, the signal intensities of the lesion, adjacent liver, and background were obtained with measurements by one radiologist (Y.Y.J.) who compared regions of interest of identical size and location on nonenhanced and gadolinium-enhanced images. Lesion signal intensity was measured by using the largest possible circular region of interest located within the lesions. Lesion signal intensity was averaged for each patient with multiple lesions of the same type. Liver signal intensities were measured with the same size circular regions of interest placed to avoid major intrahepatic vessels. Background noise was measured anterior to the abdomen (phase-encoding direction) in regions of interest with identical size and location on the nonenhanced and gadolinium-enhanced images. The SNR of the liver was calculated by dividing the liver signal intensity by the SD of the background noise. The contrast-to-noise ratio (CNR) of the lesion versus liver was calculated by dividing the difference between lesion and liver signal intensities by the SD of the background noise.
Statistical Analysis
Independent qualitative scoring of image pairs was evaluated by using the paired Wilcoxon signed rank test. The statistical significance of the data from the quantitative analysis was tested by using the paired-samples t test. A P value less than .05 was considered to indicate a statistically significant difference. To determine the interobserver variability of the qualitative analysis,
statistics were calculated to measure the degree of agreement between observers. Values up to 0.40 indicated positive but poor agreement; values of 0.410.75, good agreement; and values greater than 0.75, excellent agreement. A value of 1 indicates perfect agreement.
| RESULTS |
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values for lesion conspicuity and artifacts are summarized in Table 4; good agreement was obtained between the two readers.
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| DISCUSSION |
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Numerous investigators have noted that signal intensity differences between solid and nonsolid liver lesions are greater on fast SE images than on conventional SE images, even with similar imaging parameters, presumably because of MT suppression on fast SE images (19). The reduced signal intensity of solid lesions on fast SE images is probably the basis for the observation that contrast between solid lesion and liver may be less on fast SE images than on conventional SE images. MT-induced signal intensity reduction of solid liver lesions is a fundamental characteristic of fast SE images, based on the use of rapidly repeating refocusing pulses and on the long T1 of most liver lesions relative to that of liver (10,1215). Recent improvements in the fast SE technique have decreased acquisition time, ghost artifact, and blurring by reducing the time between echoes. However, increasing the rapidity with which refocusing pulses are repeated increases MT effects even further.
Strategies to reduce MT effects on fast SE images include eliminating or reducing the number of refocusing pulses by using echo-planar or hybrid techniques (21,22) or by reducing the flip angle of the refocusing pulses to less than 180° (23). However, echo-planar images are degraded by susceptibility and other artifacts. Flip angle reduction is only a partial solution and also would increase the prominence of stimulated echoes, increasing contrast pm T1-weighted images. A third approach is to reduce the signal intensity of the liver lesions by administering a gadolinium-based contrast agent. This strategy would also increase the signal intensity of enhancing tissues if contrast on T1-weighted images is created by stimulated echoes.
Gadolinium chelates are used commonly for hepatic MR imaging to improve detection and characterization of liver lesions (24). These agents are initially distributed in the intravascular space and then pass rapidly through capillary walls into the extracellular space of liver parenchyma and solid liver lesions. Gadolinium chelates generally enhance tumors more on delayed images, because tumors generally have a larger extracellular space than does liver. As a result, tumors are often isointense or hyperintense on delayed gadolinium-enhanced T1-weighted images. As in the brain, a gadolinium-enhanced liver tumor should recover faster from MT saturation because of its shorter T1 relaxation time, increasing its signal intensity (15).
Our results confirm that solid lesionto-liver CNR and conspicuity after gadolinium enhancement were significantly higher (P < .05) than before enhancement. Solid lesions and liver parenchyma lose substantial signal intensity because of MT effect, whereas nonsolid lesions (cavernous hemangiomas and cysts) do not. Therefore, nonsolid lesions are generally more conspicuous on fast SE images than on conventional SE images, even with similar parameters (3,12,18). Although there is a possibility that lack of statistical significance could be due to the small number of patients with nonsolid lesions, our observation that the CNR and conspicuity of nonsolid lesions did not change after administration of the gadolinium chelate is consistent with the minimal transfer of magnetization by these lesions.
Many metastases have large interstitial spaces and are therefore hyperintense on delayed-phase images. Hepatocellular carcinomas are visualized as hypervascular lesions on arterial phase images but commonly enhance less on delayed-phase images (25,26). One might expect that the conspicuity of metastasis would improve more than that of hepatocellular carcinoma because of less enhancement of the latter. Indeed, we found significantly higher conspicuity of metastases than of hepatocellular carcinoma for one reader.
One might argue that the increased contrast and conspicuity of solid lesions after gadolinium enhancement was a direct result of reduced T1. In the absence of stimulated echoes, this is not likely because solid lesions, with a typical T1 of about 1,000 msec, would recover most of their magnetization during the repetition time of 2,0002,600 msec, even without administration of a gadolinium chelate (27). In addition, we did not note improved contrast for hemangiomas, which generally accumulate more contrast material on delayed images than do solid lesions. However, a shortened T1 would increase signal due to the contribution from stimulated echoes.
Vascular pulsation artifacts can degrade fast SE images. We used gradient moment nulling in the section-select axis, and saturation bands superior and inferior to the imaging volume, to reduce the severity of flow-related artifacts (23,28). One possible concern is that vascular pulsation artifact will be increased on breath-hold T2-weighted gadolinium-enhanced fast SE images. However, we found no significant differences regarding artifact, possibly because the T1-shortening effect of the gadolinium chelate on blood had little effect on these images obtained with long repetition times. The effects of stimulated echoes on flowing blood are probably less than those on solid tissue.
Our study was limited by the small number of patients. Use of a larger number of patients may have shown a difference between images obtained with both sequences for nonsolid lesions. Also, we did not address lesion characterization and detection. The actual clinical effect of obtaining T2-weighted fast SE images after administration of a gadolinium chelate, rather than before, was not determined. However, we noted significantly improved contrast and conspicuity of solid lesions, and the acquisition of T2-weighted images after administration of a gadolinium chelate, rather than before, does not increase examination time.
The optimal parameters for T2-weighted imaging differ for detection versus characterization of liver lesions. For distinguishing solid and nonsolid lesions, more heavily T2-weighted images are recommended (2932). We routinely obtain single-shot fast SE images with an effective echo time of about 180 msec for this purpose. Because gadolinium-based contrast agents will reduce the T2 of hemangiomas and potentially decrease their signal intensity on heavily T2-weighted images, we recommend that heavily T2-weighted images for characterizing liver lesions be obtained prior to administration of a gadolinium chelate.
In conclusion, CNR and conspicuity of solid lesions on T2-weighted breath-hold fast SE images are increased after administration of a gadolinium chelate. We therefore suggest that, for detection of these lesions, T2-weighted images be obtained after, rather than before, gadolinium chelates are administered.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Abbreviations: CNR = contrast-to-noise ratio, MT = magnetization transfer, SE = spin echo, SNR = signal-to-noise ratio
Author contributions: Guarantor of integrity of entire study, D.G.M.; study concepts and design, D.G.M.; literature research, Y.Y.J.; clinical studies, D.G.M.; data acquisition, Y.Y.J.; data analysis/interpretation, D.G.M., G.A.H.; statistical analysis, Y.Y.J.; manuscript preparation and editing, Y.Y.J.; manuscript definition of intellectual content, D.G.M., Y.Y.J.; manuscript revision/review, D.G.M., G.A.H.; manuscript final version approval, D.G.M.
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