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1 Department of Radiology, National Cheng Kung University Hospital, Tainan 704,
Taiwan.
2 Department of Internal Medicine, National Cheng Kung University Hospital, 138
Sheng-Li Rd., Tainan 704, Taiwan.
3 Department of Surgery, National Cheng Kung University Hospital, Tainan 704,
Taiwan.
4 Department of Chemical Engineering, College of Engineering, National Cheng
Kung University, Tainan 704, Taiwan.
Received August 18, 2003;
accepted after revision December 7, 2003.
Address correspondence to C.-Y. Chen
(chiungyu{at}mail.ncku.edu.tw).
Abstract
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MATERIALS AND METHODS. Gallstones from 24 patients who had MRI performed before the removal of the gallstones were collected for study. The gallstones were classified either as cholesterol gallstone (n = 4) or as pigment gallstone (n = 20) according to their gross appearance and based on analysis by Fourier transform infrared spectroscopy. MRI included three sequences: single-shot fast spin-echo T2-weighted imaging, 3D fast spoiled gradient-echo T1-weighted imaging, and in-phase fast spoiled gradient-echo T1-weighted imaging. The signal intensity and the detection rate of gallstones on MRI were further correlated with the character of the gallstones.
RESULTS. On T1-weighted 3D fast spoiled gradient-echo images, most of the pigment gallstones (18/20) were hyperintense and all the cholesterol gallstones (4/4) were hypointense. The mean ratio of the signal intensity of gallstone to bile was (± standard deviation) 3.36 ± 1.88 for pigment gallstone and 0.24 ± 0.10 for cholesterol gallstone on the 3D fast spoiled gradient-echo sequence (p < 0.001). Combining the 3D fast spoiled gradient-echo and single-shot fast spin-echo sequences achieved the highest gallstone detection rate (96.4%).
CONCLUSION. Based on the differences of signal intensity of gallstones, the 3D fast spoiled gradient-echo T1-weighted imaging was able to diagnose the composition of gallstones. Adding the 3D fast spoiled gradient-echo imaging to the single-shot fast spin-echo T2-weighted sequence can further improve the detection rate of gallstones.
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The gallstones were washed with normal saline and maintained in airtight plastic bottles to avoid transformation of the gallstone structure by drying. The gallstones were classified as cholesterol stones or pigment stones according to their surface and cutting plane as described by the gallstone classification of the Japanese Study Group (1986) [11]. The gallstones were further examined by Fourier transform infrared spectroscopy on a Fourier transform infrared (FTIR) spectrometer (FTS-40, Bio-Rad) for wave number 4,000 to 400 cm–1 and a spectral resolution of 8 cm–1. Potassium bromide pellets were used to generate the background spectra. The chemical compositions were then compared to the spectra of calcium bilirubinate, calcium carbonate, and calcium palmitate.
In Vivo Imaging
MRI was performed using a field strength of 1.5 T on an MRI system (Signa
CV/i, General Electric Medical Systems) with a phased array torso coil. Two
fast spoiled gradient-echo T1-weighted images and a single-shot fast spin-echo
T2-weighted image were obtained. For in-phase fast spoiled gradient-echo
images, the parameters were TR range/TE, 175–185/4.2; slice thickness, 8
mm; gap, 2 mm; and flip angle, 90°. For 3D fast spoiled gradient-echo
images, the parameters were TR/TE, 5.9/1.2; slice thickness, 6 mm; 3-mm
overlap between each image; and flip angle, 10°. For single-shot fast
spin-echo T2 images, the parameters were TR range/TE range,
20,000–25,000/90–100; slice thickness, 8 mm; and gap, 2 mm. The 3D
fast spoiled gradient-echo images were acquired with fat saturation, and the
in-phase fast spoiled gradient-echo images were not. All the sequences used a
field of view as adjusted by the patients' respective body sizes and a 256
x 168 matrix. The gallstone images obtained using the different
sequences were analyzed for the presence and signal intensity of
gallstones.
In Vitro Imaging
The gallstones were placed in a normal saline suspension in individual
plastic bottles and embedded in water-immersed custom floral foam as a body
phantom for MRI. In vitro MRI used the same sequences and parameters as the
set for the in vivo MRI except that the slice thickness was 5 mm and an
additional set of in-phase fast spoiled gradient-echo images with fat
saturation was also obtained.
The gallstones were first pulverized and desiccated before the MRI was performed to analyze the contribution of water content in the signal intensity of gallstones on MRI. The homogeneous gallstone powder was placed individually in the plastic Eppendorf tube and embedded in water-immersed custom floral foam as a body phantom for MRI. The setting used for the MRI was the same as that described for the in vitro study. MRI was repeated after adding normal saline to the desiccated gallstone powder to confirm the influence of water on the signal intensity rather than that of any structural change during the process of desiccation. The appearance and signal intensity of the gallstones were recorded for further analysis.
Measurement of Signal Intensity
Quantitative assessment of the signal intensity on T1- and T2-weighted
sequences was obtained through operator-defined regions of interest. The
gallstone signal intensity was measured and compared with the intensity of the
gallbladder bile, resulting in a stone–bile signal intensity ratio for
each gallstone. Signal intensity was measured at the bile of the dilated
common bile duct in three patients who underwent cholecystectomy earlier. If
the intensity of a gallstone's magnetic resonance signal varied throughout its
structure, it was measured at its most intense region.
In vitro measurement of signal intensity was similar to the in vivo study except that the signal intensity was measured either at the gallstones and surrounding saline or at the gallstone powder and the water-immersed floral foam phantom.
Statistical Analysis
The value of signal intensity ratio was expressed as mean ± 1 SD.
The differences in the signal intensity ratio between the cholesterol and
pigment gallstone groups were examined by the Mann-Whitney U test.
The detection rates of gallstones on different MRI sequences were compared
using the chi-square test. A p value of less than 0.05 was considered
to be statistically significant. The statistical calculations were computed
using SPSS version 8.0 (Statistical Package for the Social Sciences) for
Windows (Microsoft).
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As shown in Table 1, 90% and 30% of the pigment gallstones were hyperintense on the in vivo T1-weighted 3D fast spoiled gradient-echo (Fig. 1A) and in-phase fast spoiled gradient-echo images, respectively, and all the cholesterol gallstones were hypointense on the T1-weighted images (Figs. 2A and 2B). All the gallstones appeared as hypointensities on the T2-weighted single-shot fast spin-echo images (Figs. 1C and 2C). The in vivo (Figs. 1A, 1B, 1C and Figs. 2A, 2B, 2C) and in vitro (Figs. 1D, 1E, 1F, 1G and Figs. 2D, 2E, 2F, 2G) images of gallstones were similar but differed in that more pigment gallstones were hyperintense on the in vitro T1-weighted in-phase fast spoiled gradient-echo images.
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As listed in Table 2, the contrast of signal intensity between the pigment gallstones and the background was prominent on either the in vivo or the in vitro 3D fast spoiled gradient-echo images and became less prominent on the T1-weighted in-phase fast spoiled gradient-echo images with and without fat saturation. The signal intensity of cholesterol gallstones was lower than that of the background on both T1- and T2-weighted MR images. The mean ratios of stone-to-background signal intensities of pigment and cholesterol gallstones were therefore significantly different on the 3D fast spoiled gradient-echo and in-phase fast spoiled gradient-echo T1-weighted images but were similar on the T2-weighted single-shot fast spin-echo images.
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Table 3 shows the effect of the water content on gallstone MRI. The desiccated powders of all cholesterol and pigment stones were hypointense on T1-weighted imaging. The intensities of the pigment gallstone powders on T1-weighted images were so greatly enhanced after adding normal saline that the mean intensity of pigment gallstones was 4.36 and 3.86 times greater, respectively, to that of body phantom on 3D fast spoiled gradient-echo and in-phase fast spoiled gradient-echo sequences. However, the mean intensity of cholesterol gallstone was only slightly enhanced after the addition of normal saline with a mean signal intensity ratio of stone-to-body phantom of approximately 1 on T1-weighted images. Both the pigment and cholesterol gallstone powders were hypointense on T2-weighted images, and the signal intensities were lower than that of the body phantom, whether before or after the addition of normal saline.
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Table 4 shows the results of MRI diagnosis of gallstone using different MRI sequences. The cholesterol gallstones exclusively occurred in the gallbladder in our collections and were visualized as filling defects on all three MRI sequences (Figs. 2A, 2B, 2C). The T2-weighted single-shot fast spin-echo imaging showed pigment gallstone as a filling defect and was good in detecting those gallbladder stones. The T1-weighted 3D fast spoiled gradient-echo imaging presented the pigment gallstones as hyperintense areas and was good in detecting those common bile duct stones (Fig. 1A). The T1-weighted 3D fast spoiled gradient-echo MRI missed a gallbladder stone and the T2-weighted single-shot fast spin-echo MRI missed two common bile duct stones. Moreover, both the T1- and T2-weighted MRI missed detecting a case of intrahepatic duct stones, which were isointense pigment stones 5 mm in diameter and appearing in a nondilated bile duct. Because more than half the pigment gallstones appeared isointense on T1-weighted in-phase fast spoiled gradient-echo images (Table 1), the in-phase fast spoiled gradient-echo imaging was not good for the detection of pigment gallstone. Combining the 3D fast spoiled gradient-echo and the single-shot fast spin-echo MRI sequences achieved the highest rate of gallstone detection.
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T2-weighted imaging has been considered superior to T1-weighted imaging in detecting bile duct stones because most of the gallstones are isointense on T1-weighted MR images [13]. Although only some gallstones have been reported to be hyperintense on T1-weighted imaging [5–10], a considerable number of stones have appeared as hyperintensities on our T1-weighted imaging. Gallstones of hyperintensity on T1-weighted images have been found to be related to stones having brown to black cross sections or a salt-and-pepper appearance [6, 10]. These stones, according to the gallstone classification of the Japanese Study Group [11], should be classified as pigment gallstones. As seen in our study, the intensity ratio of gallstone to bile or to normal saline of the T1-weighted imaging was significantly higher for pigment gallstones than for cholesterol gallstones. These findings show that the hyperintense gallstones on T1-weighted images were pigment gallstones and cholesterol gallstones were exclusively hypointense on T1-weighted imaging.
Differentiation of pigment and cholesterol gallstones was once important 10–20 years ago, when gallstone dissolution therapy was popular for patients with gallbladder stones. At that time, diagnosis of the composition of the gallstone was important in predicting the success of gallstone dissolution and in choosing the solvent for gallstone dissolution. The advent of laparoscopic cholecystectomy, however, has changed that. Currently, few patients with gallstones are treated with dissolution therapy. Nevertheless, because of the different consistencies of cholesterol and pigment gallstones, the differentiation of gallstone composition may still have a clinical impact when dealing with endoscopic mechanical lithotripsy for big common bile duct stones. On such an occasion, the big pigment gallstone can be easily crushed by a mechanical lithotripter and retrieved, whereas the presence of big cholesterol gallstones usually implies a difficult-to-treat stone because they are harder than pigment stones and endoscopic lithotripsy may fail.
Ukaji et al. [10] studied the in vitro images of gallstones and considered that the hyperintensity of pigment gallstone on T1-weighted images was caused by the presence of metal ions in the pigment stones. These metal ions behave as paramagnetic ions, shortening the T1 relaxation time of water protons, and as such, stones containing these ions appeared as hyperintense areas on T1-weighted images. The presence of water, therefore, plays a key role in determining the intensity of gallstones on MRI. This theory was further tested and supported by our study, showing that all pigment gallstones became signal void on T1-weighted imaging after desiccation, whereas the hyperintensity of pigment gallstones was restored after adding normal saline.
We found that most of the pigment gallstones were hyperintense on the T1-weighted 3D fast spoiled gradient-echo images, although only one third of them were hyperintense on the T1-weighted in-phase fast spoiled gradient-echo images. Because the 3D fast spoiled gradient-echo images were acquired with fat saturation and the in-phase fast spoiled gradient-echo images were not, the higher intensity of gallstone on 3D fast spoiled gradient-echo images may be caused by fat saturation itself, which increased the apparent brightness of water-bearing stones. Such inference, however, has been discounted because the in vitro in-phase fast spoiled gradient-echo images showed similar image and intensity ratio acquired either with or without fat saturation. The 3D fast spoiled gradient-echo MRI sequence differs from the in-phase fast spoiled gradient-echo sequence not only in the thickness of the slice but also in the TE and TR. As seen in the previous ferumoxides experiment, the short TE of 3D fast spoiled gradient-echo sequence may reduce the susceptibility and short transverse relaxation effect of the metal ions and therefore increase the signal of pigment gallstones [14]. The TR of the 3D fast spoiled gradient-echo sequence being shorter than the in-phase fast spoiled gradient-echo sequence may contribute to a suppression of the background signal and result in improved visualization of the longitudinal effect of gallstones containing metal ions [14]. Because the 3D fast spoiled gradient-echo sequence is not used for routine MRI diagnosis of gallstone, its application in our study should account for the higher incidence of hyperintense gallstones in our study than in other reports.
MR cholangiography and T2-weighted MRI detect gallstones indirectly by showing them as filling defects. However, several pitfalls are associated with them. First, other types of intraluminal filling defects, such as intraductal tumor, blood clot, or gas bubble (pneumobilia), can mimic gallstones and may be difficult to differentiate [15]. Second, gallstones impacted at the ampulla may be missed on T2-weighted imaging because of the lack of bile surrounding the stone and, hence, no filling defect will appear on the images [15]. These pitfalls can be avoided by using T1-weighted 3D fast spoiled gradient-echo imaging because it reveals pigment gallstones directly as hyperintense areas on images rather than just as filling defects. This characteristic of T1-weighted 3D fast spoiled gradient-echo imaging explains why the 3D fast spoiled gradient-echo sequence is better than the single-shot fast spin-echo sequence for MRI in terms of diagnosing common bile duct stones in our study.
In summary, our study shows the MRI characteristics of cholesterol and pigment gallstones. In addition to recognizing a gallstone as a filling defect on T2-weighted single-shot fast spin-echo imaging, the cholesterol and pigment gallstones can be readily differentiated because most pigmented stones are bright, whereas cholesterol stones are dark on 3D fast spoiled gradient-echo T1-weighted imaging. The 3D fast spoiled gradient-echo T1-weighted imaging is as good as T2-weighted single-shot fast spin-echo imaging in diagnosing gallstones and can even be better when applied to bile duct stones. Common bile duct and intrahepatic duct stones are frequently pigment gallstones and are prevalent in many areas of Asia. We recommend a combined use of 3D fast spoiled gradient-echo and single-shot fast spin-echo sequence for routine MRI of gallstones.
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