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1
Department of Medical Imaging, Toronto General Hospital, University Health
Network, 200 Elizabeth St., Toronto, Ontario, M5G 2C4 Canada.
2
Present address: Hospital Clinico Universidad de Chile, Servicio de
Radiologia, Santos Dumont 999, 4t. piso sector C, Santiago, Chile.
3
Department of Medical Biophysics, University of Toronto, Imaging Research,
Sunnybrook and Women's College Health Science Centre, 2075 Bayview Ave.,
Toronto, Ontario, M5G 2C4 Canada.
Received November 15, 1999;
accepted after revision September 15, 2000.
Address correspondence to S. R. Wilson.
Abstract
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SUBJECTS AND METHODS. Eighty patients with suspect biliary disease had conventional sonography and tissue harmonic imaging with an ATL 3000 or 5000 scanner in a 6-month interval. Final diagnoses included malignant biliary obstruction (n = 30), choledocholithiasis (n = 16), sclerosing cholangitis (n = 4), normal or nonobstructed ducts (n = 16), and miscellaneous conditions (n = 14). Similar images were taken with each technique in terms of projection, field of view, focal zone selection, and evidence of disease. Two separate observers blinded to patient data and technique reviewed and graded images individually for the appearance of the lumen of the bile ducts, the length of the visible duct, the appearance of the duct wall, the presence of any intraluminal masses, and the appearance of associated acoustic shadows. Images were graded from zero to 3, with 3 being the best.
RESULTS. The median of the 546 tissue harmonic images was one grade higher than the median for the corresponding conventional images (p < 0.0001). Improvements with tissue harmonic imaging included better sharpness of the duct walls (p < 0.01), a clearer lumen (p < 0.0001), identification of a longer length of the common bile duct (p < 0.0001), and improved detection of intraluminal masses (p < 0.006). Acoustic shadows were better defined and blacker with tissue harmonic imaging (p < 0.007).
CONCLUSION. Improvement in contrast and reduction of side lobe artifacts with tissue harmonic imaging enhance visualization of the biliary ducts. Tissue harmonic imaging is now our routine technique for bile duct examination.
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Sonography is well established for preliminary examination of the patient with symptomatology suggestive of biliary disease. With state-of-the-art sonographic equipment without harmonic capability, detection of dilated biliary ducts allows differentiation of surgical or obstructive jaundice from medical disease [5]. Prediction of the correct level of biliary obstruction on sonography is excellent with reported accuracies in excess of 90% [5,6,7,8]. Reports are somewhat more variable in identifying the cause of obstruction. Detection of choledocholithiasis is reported with accuracies as low as 32% [9] and as high as 71% [10]. Meticulous technique, the addition of Doppler sonography, and ever improving sonographic equipment have all contributed to significant advances in sonographic performance for the assessment of the biliary tract over the last two decades. Objectives today include not only correct prediction of the presence and level of biliary obstruction but also the detection and staging of malignant neoplasms [11,12,13].
Problems that may be encountered in the performance of biliary sonography are largely related to patient body habitus. In a large patient, the distal common bile duct may be deep in the abdomen, hidden by both adipose tissue and overlying structures. The position of the distal common bile duct, posterior to the sweep of the duodenum, makes gas artifact from the gut another potential source of error. Furthermore, the bile duct, as a cystic structure, is often seen to contain low-level artifactual echoes in its near field caused by both reverberation and side lobe artifact. Although identification of these artifacts is readily achieved in a large viscus such as the gallbladder or the urinary bladder, in a small structure, such as the common bile duct, these artifacts may be a source of misinterpretation. Therefore, there is strong motivation to improve the capability of sonography in the study of the biliary ducts.
Tissue harmonic imaging is reported to improve the visualization of fluid-filled or cystic structures with reduction of artifact and increased contrast resolution. Cardiology experience has shown that tissue harmonic imaging improves the assessment of the fluid-filled cardiac chambers with clearer depiction of the endocardial surfaces [4]. We describe our experience with tissue harmonic imaging in the evaluation of much smaller cystic structures, the biliary ducts.
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All diagnoses were confirmed with further laboratory tests, pathology, or imaging. Follow-up assessment was for confirmation of the diagnosis only. Of the 30 patients with malignant biliary obstruction, sonography correctly identified and diagnosed 17 of the 18 pancreatic head carcinomas, all five cholangiocarcinomas, ductal metastatic disease in one patient, and malignant obstruction caused by metastatic lymph nodes at the porta hepatis in one patient. In the remaining pancreatic head carcinoma and in all the carcinomas of the ampulla of Vater, sonography correctly indicated distal extrahepatic biliary obstruction, for which further evaluation for a potential small periampullary neoplasm was recommended in the final report. CT did show the missed cancer of the pancreas. The tumors of the ampulla of Vater were not seen on imaging before surgery. All bile duct stones seen on sonography in 16 patients were confirmed by endoscopic retrograde cholangiopancreatography.
Sonographic Technique and Assessments
Each patient had assessment of the biliary tract with conventional
sonography and tissue harmonic imaging. All scans were obtained on
state-of-the-art sonographic equipment, with harmonic imaging capability, ATL
3000 or ATL 5000 scanner (Advanced Technology Laboratories, Bothell, WA).
Sonographic probes were either C4-2 MHz or C5-2 MHz. Any one of several
certified sonography technologists and sonography-dedicated physicians in our
department initially obtained scans. Similar images in terms of projection and
technical parameters were taken with each modality. These images included the
right and the left intrahepatic ducts, the hepatic ductal confluence at the
porta hepatis, the common hepatic duct, and the common bile duct in its upper,
mid, and distal portions. Extra images to show any identified disease were
obtained with both modalities. Both sets of images were made by the same
sonographer at the same time.
We chose pairs of the representative best images of the biliary ducts in each patient, taken in the same projection, using similar techniques with conventional imaging and tissue harmonic imaging. Images were selected to show the longest length of the common bile duct, the duct walls, and any biliary disease. All images of the bile ducts were cropped to exclude annotation of the modality used, the date of image acquisition, and patient identity. The images were randomly arranged as single images in a computer file so that the tissue harmonic imaging and the conventional image from a single case were not together. Individual images were then reviewed blindly by two radiologists, each with more than 5 years' experience in abdominal sonography. In all 80 patients, images were assessed for the appearance of the lumen of the bile ducts, the length of the visible common bile duct, and the appearance of the walls of the bile ducts. In the 17 patients with intraluminal masses (16 stones and one intraductal tumor), the images were also assessed for the detection of the intraluminal masses. In the 16 patients with choledocholithiasis, the appearance of any associated acoustic shadows was also assessed, making a total of 273 grades (80 + 80 + 80 + 17 + 16) per reviewer for each of the modalities, tissue harmonic imaging and conventional imaging. Each image was graded from zero to 3, with 3 being the best grade, according to criteria given to the blinded reviewer and summarized in Table 1. The results of the unpaired data grading were analyzed with the Wilcoxon's signed rank test, the Mann-Whitney U-test, and Fisher's exact test.
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Lumen Visualization
In three quarters of all cases, lumen visualization with tissue harmonic
imaging improved when compared with conventional imaging (61 [76%] of 80
images for reviewer 1; 59 [74%] of 80 images for reviewer
2;p<0.0001, Wilcoxon's signed rank test) (Figs.
5A,5B
and
6A,6B).
As a group, the tissue harmonic images were rated with higher grades than the
conventional images by both reviewers (median grade 3 versus median grade 2,
p < 0.0001, Mann-Whitney U-test). There was excellent concordance
between the two reviewers, who agreed on the grade in 142 (89%) of 160
images.
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Assessment of Length
In 28 (35%) of 80 cases, a greater length of duct was visualized with
tissue harmonic imaging than with conventional imaging (p <
0.0001, Wilcoxon's signed rank test) (Fig.
7A,7B).
As a group, a greater length of duct was seen in tissue harmonic images than
in conventional images (p < 0.03, Mann-Whitney U-test). The two
blinded reviewers agreed on the grade in 152 (95%) of 160 images.
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Visualization of Duct Walls
Wall visualization in 67 (84%) of 80 cases was the same with conventional
imaging and tissue harmonic imaging (Fig.
8A,8B).
In approximately 11 (14%) of 80 cases, both reviewers considered visualization
improved with tissue harmonic imaging (p < 0.01, Wilcoxon's signed
rank test) The two blinded reviewers agreed on the grade in 151 (95%) of 160
images.
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Intraluminal Mass Delineation
Of the 17 patients (21%) in whom a stone (Fig.
9A,9B)
or intraductal tumor (Fig.
10A,10B)
was seen, tissue harmonic imaging improved visualization in an average of
eight patients (47%, p < 0.01; Wilcoxon's signed rank test, both
reviewers). As a group, the tissue harmonic images were rated with higher
grades than the conventional images by both reviewers (p < 0.005,
Mann-Whitney U-test). The reviewers agreed on the grade of the images in 26
(76%) of 34 cases. Acoustic shadowing was seen more clearly in seven (41%) of
17 cases with tissue harmonic imaging than with conventional imaging
(p < 0.02, Wilcoxon's signed rank test) (Fig.
9A,9B).
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We found that in the patient in whom visualization of the most distal portion of the common bile duct was difficult on conventional imaging, tissue harmonic imaging showed a longer length of the duct with relative ease. We attribute this advantage to the improved contrast resolution on tissue harmonic imaging between the black duct lumen and the white or gray surrounding soft tissue and to the artifact reduction in the difficult patient. Whereas on conventional images the duct might be only a few shades of gray different from the surrounding tissue, the differences were magnified on tissue harmonic images.
The duct lumen similarly appeared virtually echo-free on the tissue harmonic images, making it easier to assess. Its length, its course, and filling defects, if any, were more easily and quickly appreciated. In normal-caliber ducts, this advantage of tissue harmonic imaging is not as evident because the small lumen does not frequently show significant artifactual echo even on a conventional image (Fig. 11A,11B).
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We did not record prospectively the patient's body weight and height to determine if improved imaging with tissue harmonic imaging would correlate with large body habitus. It is our subjective impression, however, that the improvement in biliary imaging is greatest in the patient who is large in whom artifactual echoes frequently fill the bile duct lumen and in whom tissue attenuation makes visualization difficult. This apparent benefit for tissue harmonic imaging in the difficult-to-scan patient has a plausible explanation. As the harmonic signal is generated in the body, there is a single transmission of the sonographic signal through the body wall (Figs. 3 and 4). In conventional imaging, the sonographic signal passes through the body wall twice, on its way to the target and on its way back to the transducer. Therefore, in the large patient with a thick and attenuating body wall, there is greater beam distortion and greater artifact production on the conventional image than there is on tissue harmonic imaging.
The apparent advantage of tissue harmonic imaging in the difficult-to-image patient is, however, offset by a reduction of penetration with tissue harmonic imaging compared with conventional imaging. Tissue harmonic imaging relies on the detection of higher frequency components of the echo and, therefore, suffers more noticeably from attenuation. In spite of this potential limitation of tissue harmonic imaging for scanning large patients, the advantages afforded by tissue harmonic imaging seem to offset any disadvantages.
We believe the reverse of this situation is also true. In many thin patients, particularly in those who afford an excellent scan, the bile duct lumen can appear black and echo-free even with conventional imaging. Therefore, the advantages of tissue harmonic imaging, if any, are minimized.
Although the preference for tissue harmonic imaging was similar throughout our study, our real-time experience suggests that the most dramatic advantage for tissue harmonic imaging is in the evaluation of stone disease. In three of our patients, tiny intraductal stones were seen easily on the real-time examination with tissue harmonic imaging and were seen on the conventional imaging only after we knew of their presence from the harmonic portion of the scan. In these three patients, however, the frozen conventional images provided to the blinded reviewers did not show the abnormality convincingly, and images were given a grade of zero, intraluminal mass not seen, in five of the six evaluations. These stones were all recognized on the blinded review of tissue harmonic images. Furthermore, tissue harmonic imaging improves both the detection of the actual intraluminal mass and the appreciation of the acoustic shadow behind a stone. Indeed, improved detection of acoustic shadowing on tissue harmonic imaging makes the shadow behind a stone the first thing that the radiologist may appreciate while actually performing the real-time examination. This advantage is of particular benefit in the detection of a tiny stone in the distal common bile duct (Fig. 12A,12B).
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Our preference for tissue harmonic imaging over conventional sonography for the evaluation of the biliary ducts did not always extend to the remainder of the examination in our study population. In patients with malignant neoplastic obstruction of the bile ducts, we routinely preferred the conventional technique for the actual examination of the neoplasm. We think that this preference relates, at least in part, to both better resolution and a broader gray-scale range with conventional imaging when compared with current tissue harmonic imaging. The benefits of tissue harmonic imaging would not, therefore, be expected to show an advantage extending to the examination of neoplasms that were all solid and often poorly defined. By comparison, Shapiro et al. [14] studied the pancreas in 60 patients and showed a preference for tissue harmonic imaging over conventional imaging in terms of better penetration, detail, and image quality. Solid-organ examination with conventional imaging was not tested in our protocol. However, our experience to date suggests that many solid organs, such as the liver, benefit from the broader gray-scale range and resolution of conventional imaging. This difference in our results compared with those of Shapiro et al. may be related to the use of different equipment.
Harmonic imaging involves several inherent trade-offs. The scattered harmonic echoes are relatively weak when compared with conventional echoes so that electronic noise may be an issue in some situations. Also, to separate harmonic echoes from conventional echoes and to minimize electronic noise, transmit and receive bandwidths are reduced in harmonic imaging. This change increases axial blurring in the harmonic image [15]. Because of these trade-offs, the choice of whether to use conventional or harmonic imaging must be assessed separately for different imaging conditions. A recently developed method for harmonic imaging known as pulse-inversion imaging [16] may improve this situation. Pulse-inversion images offer all the advantages of tissue harmonic imaging at full resolution, although at a somewhat reduced frame rate.
Our study was not performed to compare the final diagnoses obtained with tissue harmonic imaging with those of conventional sonography. Rather, we determined that tissue harmonic imaging has a high subjective acceptance and, in fact, is now routinely preferred by our sonographers for biliary tract assessment. Inherent in tissue harmonic imaging is an improvement in contrast with loss of resolution. Therefore, when tissue harmonic imaging is turned on, there is a subjective impression that the image looks blurry in comparison with a conventional image. Biliary tract evaluation, however, does not require the extensive gray-scale performance that is critical for many other aspects of sonography. The improvement in contrast is far more beneficial in the detection of the tiny mural abnormality and certainly in the detection of the bile duct stone that is located in a cystic tubular structure such as the common bile duct.
In conclusion, our study shows a clear advantage for tissue harmonic imaging in the examination of the biliary ductal system with sonography. Images judged to be superior with tissue harmonic imaging showed a longer length of the common bile duct; a cleaner bile duct lumen, without artifactual echoes within; sharper bile duct walls; more evident intraluminal filling defects; and particularly sharper and more echo-free acoustic shadows distal to bile duct stones. We believe that the ease with which the duct can be seen and followed with this modality will afford an opportunity for a more rapid and successful examination even on the ill or large patient. It is our belief that improved diagnosis is possible with tissue harmonic imaging and that it should facilitate improved biliary assessment with sonography, even by the less experienced sonographer.
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