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1 Division of Digestive Organs, Department of Cancer Survey, Osaka Medical
Center for Cancer and Cardiovascular Diseases, 1-3-3, Nakamichi, Higashinari,
Osaka, 537-8511, Japan.
2 Department of Diagnostic Radiology, Osaka Medical Center for Cancer and
Cardiovascular Diseases, Osaka, 537-8511, Japan.
Received July 5, 2001;
accepted after revision November 12, 2001.
Supported in part by a grant from the Foundation for Promotion of Cancer
Research.
Abstract
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MATERIALS AND METHODS. IV contrast-enhanced pancreatic sonography (dynamic sonography) with Levovist was performed in 43 patients with pancreatic mass lesions (32 with pancreatic adenocarcinomas, four with inflammatory pancreatic masses, three with islet cell tumors, two with serous cystadenomas, one with a solid and cystic tumor, and one with metastatic pancreatic cancer). We calculated a contrast index using a time—intensity curve: contrast index equals elevation of intensity in the tumor divided by elevation of intensity in the pancreatic parenchyma. We classified the tumors into three groups according to the contrast index: a slightly enhanced group (contrast index < 0.5), a moderately enhanced group (contrast index = 0.5-1.5), and a well-enhanced group (contrast index > 1.5), and we compared these results with those from dynamic CT.
RESULTS. The contrast indexes of 32 adenocarcinomas, four inflammatory pancreatic masses, three islet cell tumors, two serous cystadenomas, one solid and cystic tumor, and one metastatic tumor were, respectively, 0.12 ± 0.095 (mean ± SD), 0.54 ± 0.420, 1.74 ± 0.555, 1.09 ± 1.380, 1.67, and 2.07. Thirty-five tumors, including all 32 adenocarcinomas, were classified in the slightly enhanced group, three were classified in the moderately enhanced group, and five were classified in the well-enhanced group. In 93% (40/43) of tumors, the grade of enhancement on dynamic sonography was closely correlated with the grade of enhancement on dynamic CT.
CONCLUSION. Dynamic sonography can assist in the characterization of pancreatic tumors.
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Recently, IV contrast agents for sonography have become commercially available. Also, a pulse inversion harmonic imaging technique has been developed, whereby harmonic echoes caused by microbubble vibration or disruption have become detectable [2]. We performed sonography using pulse inversion harmonic imaging with the contrast agent Levovist (D-galactose; Schering, Berlin, Germany) and evaluated the vascularity of pancreatic tumors for differential diagnosis. We compared the results with those from dynamic CT.
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Seven patients with ductal adenocarcinoma, one patient with islet cell carcinoma, and one patient with a solid and cystic tumor underwent resection, and their diagnoses were histologically confirmed. The diagnoses of two patients with serous cystadenoma were confirmed by fine-needle biopsy. The remaining 32 patients each underwent three imaging studies (CT, MR imaging, and endoscopic retrograde cholangiopancreatography) and a pancreatic juice cytology for differentiation.
Dynamic Sonography
Levovist was injected through a brachial vein as a bolus (within 20 sec) at
300 mg/mL x 0.1 mL/kg body weight, followed by a 5-mL flush of 0.9%
saline solution. We used a sonographic scanner (HDI-5000; ATL Ultrasound,
Bothell, WA) with a C5-2 curvilinear array transducer and the pulse inversion
harmonic imaging mode, which transmits 2.5-MHz sound and receives 5.0-MHz
sound. The dynamic study of contrast-enhanced imaging was performed following
the protocol for liver tumors
[3]. We observed the pancreatic
tumors and parenchyma from 10 sec before to 90 sec after administration of
Levovist, with a frame rate synchronized to ECG (one frame per one beat) at a
low mechanical index (0.4). The dynamic range was set at 150 dB. All raw data
were digitally stored. Measurement was performed quantitatively by computer
(HDI-Lab system software; ATL Ultrasound).
On all sonograms, 5-mm circular regions of interest were placed in the central area of the tumor and adjacent pancreatic parenchyma. The mean intensity of each of the regions was measured before and after enhancement and a time—intensity curve was drawn. To evaluate the effect of enhancement by Levovist, we calculated the contrast index (contrast index = elevation of intensity in the tumor / elevation of intensity in the pancreatic parenchyma). Elevation of intensity was the difference of the intensity before enhancement and at maximal intensity. For example, a tumor with a contrast index of 1.0 enhances to the same extent as pancreatic parenchyma, a tumor with a contrast index of 0.5 enhances half as much as parenchyma, and a tumor with a contrast index of 2.0 enhances twice as much.
We classified tumors in three groups according to the contrast index: a slightly enhanced group (contrast index < 0.5), a moderately enhanced group (contrast index = 0.5-1.5), and a well-enhanced group (contrast index > 1.5). We compared the contrast index results with the final diagnosis of each tumor and the results from dynamic CT.
Dynamic CT
Dynamic CT was performed in all subjects using one of two CT scanners (X
Vigor, Toshiba, Tokyo, Japan, or Somatom Plus, Siemens, Erlangen, Germany).
Scanning using 120 kVp and 250 mA started 40 sec after the peripheral
injection of iopamidol 300 mg I/mL (Iopamiron 300; Schering Japan, Osaka,
Japan) at a rate of 2.5 mL/sec of 100 mL. The scanning parameters were
collimation, 5 mm; table speed, 5 mm/sec; reconstruction pitch, 5 mm; and scan
time, 40 sec. The enhancement patterns were classified as one of three types:
Hyperdense mass was defined as a mass showing greater density than the
pancreatic parenchyma; isodense mass was a mass showing equal density to the
pancreatic parenchyma; and hypodense mass was a mass showing less density than
the pancreatic parenchyma.
Written informed consent was obtained from all patients for both the dynamic sonography and the dynamic CT examinations.
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Contrast Index of the Tumors
The contrast index of each of the tumors is shown in
Figure 1. Thirty-five tumors
(32 adenocarcinomas, two inflammatory pancreatic masses, and one serous
cystadenoma) were classified as slightly enhanced, three tumors (two
inflammatory pancreatic masses and one islet cell tumor) were classified as
moderately enhanced, and five tumors (two islet cell tumors, one serous
cystadenoma, one solid and cystic tumor, and one metastatic tumor) were
classified as well enhanced.
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In all 32 patients with ductal adenocarcinoma, the tumor was not as enhanced as the surrounding pancreatic parenchyma (Fig. 2A,2B,2C,2D). The contrast index ranged from 0.01 to 0.45 (mean, 0.12 ± 0.095), and all of these tumors were classified as slightly enhanced. Two of the four inflammatory pancreatic masses were classified as slightly enhanced, and the other two were classified as moderately enhanced. The contrast index ranged from 0.11 to 0.99 (mean, 0.54 ± 0.420). Two of the three islet cell tumors were classified as well enhanced (Fig. 3A,3B,3C,3D), and the remaining one was classified as moderately enhanced. The contrast index ranged from 1.13 to 2.20 (mean, 1.74 ± 0.555). The contrast index of each of the two serous cystadenomas was 0.11 and 2.07. One was classified as slightly enhanced, and the other one was classified as well enhanced. The solid and cystic tumor was partially enhanced and was classified as well enhanced. The metastatic tumor from renal cell carcinoma was classified as well enhanced.
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Comparison with CT Findings
Figure 4 shows the
correlation between the contrast index on dynamic sonography and the
enhancement effect on dynamic CT. All 32 adenocarcinomas were classified as
hypodense masses on dynamic CT and were classified as slightly enhanced on
dynamic sonography. In 93% of tumors (40/43), the grade of enhancement on
dynamic sonography and dynamic CT corresponded well. A discrepancy was
observed in three cases (one islet cell carcinoma, one serous cystadenoma, and
the solid and cystic tumor).
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More recently, pulse inversion harmonic imaging has been developed. The improved sensitivity to the contrast agent of this technique allows better assessment of the vascularity of tumors [2]. Using a contrast agent in combination with pulse inversion harmonic imaging is useful for the characterization of liver tumors because the technique makes possible the visualization of blood supply or the vascularity of the liver parenchyma or liver tumors [3]. We applied this method to pancreatic tumors and correlated the results with CT findings for the characterization of the tumors. In 93% (40/43) of tumors, the finding with dynamic sonography correlated well with dynamic CT findings.
Ductal adenocarcinoma of the pancreas usually shows a hypoechoic mass with obscure margins on unenhanced sonography. After contrast enhancement, the adenocarcinomas in our study showed less enhancement than the normal pancreatic parenchyma, the margins of the tumors became well demarcated, and the character of hypovascularity was clearly shown.
Inflammatory pancreatic masses also present as hypoechoic lesions with relatively discrete margins, and they are difficult to differentiate from ductal adenocarcinoma. Koito et al. [1] reported that contrast-enhanced sonography with arterial injection of carbon dioxide microbubbles could help differentiate an inflammatory pancreatic mass from a ductal adenocarcinoma and that contrast-enhanced sonograms showed a significantly higher sensitivity and accuracy rate than CT or angiography in the differentiation of pancreatic adenocarcinomas from inflammatory pancreatic masses. However, this method of contrast-enhanced sonography is invasive and complex. In our series, two of the four inflammatory pancreatic masses were classified as moderately enhanced on dynamic sonography, making it less likely that they represented adenocarcinoma. But the remaining two were classified as slightly enhanced on dynamic sonography, making them impossible to differentiate from ductal adenocarcinoma. These two masses were also classified as hypodense on dynamic CT; other laboratory data did not show an elevation of serous amylase or inflammatory reaction. For these masses as well, it was difficult to differentiate ductal adenocarcinoma from inflammatory pancreatic mass.
Most islet cell tumors are hypervascular and appear hyperintense compared with surrounding pancreatic tissue in both arterial and portal venous phase CT. In our study, two benign islet cell tumors were well enhanced on both dynamic sonography and dynamic CT. The remaining one was also revealed as hyperdense on dynamic CT. However, with dynamic sonography, the tumor was only slightly more enhanced than the parenchyma, the Contrast Index was not higher than 1.5, and it was classified as moderately enhanced.
We found two cases in which the results of dynamic sonography were substantially different from those of dynamic CT. We cannot explain this discrepancy, but both of these masses contained cystic and solid components. We theorize that the echo signals are compressed in dynamic sonography and enhanced at the margin between the solid and cystic components and that, through real-time imaging, the most dramatic regions of area were selected for evaluation. In distinction, when we used dynamic CT, the volume average of the hypodense cystic portion served to decrease the overall density of the lesion.
Metastatic tumors show various appearances according to the character of the primary lesions. A case of metastatic tumor from renal cell carcinoma was included in our study, and the tumor was well enhanced on both dynamic sonography and dynamic CT.
The contrast agent for sonography did not cause an allergic reaction (as is often the case with iodic contrast media) and it did not influence renal function.
In summary, our study revealed three points: First, contrast enhancement increases lesion detectability. Lesions that are subtle without contrast become more obvious and well defined with contrast. Second, a strong correlation exists between the results of dynamic sonography and of dynamic CT. This enhancement characteristic permits evaluation of the vascularity of lesions, which, presumably, will narrow the differential diagnosis. Third, no allergic reaction or renal insult is reported with this type of contrast agent [13,14,15], whereas with CT, such responses are a limiting factor.
In conclusion, dynamic sonography with Levovist using pulse inversion harmonic imaging reveals the vascularity of pancreatic tumors, and it is useful for the differential diagnosis of pancreatic tumors. The limitation of this method is that it is applicable only for patients in whom the pancreatic tumor and parenchyma can be clearly observed in a single view.
Acknowledgments
We thank Kunihiro Chihara of Nara Institute of Science and Technology for
useful advice.
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=
inflammatory pancreatic mass, 
= islet cell tumor, 
= serous
cystadenoma, 
= solid and cystic tumor, 
= metastatic tumor.