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Isoattenuating Pancreatic Adenocarcinoma at Multi–Detector Row CT: Secondary Signs¹

¹ From the Department of Radiology, Lucas MRS Center, Stanford University, Stanford, Calif. Received July 26, 2001; revision requested September 24; final revision received March 4, 2002; accepted March 28. R.W.P. supported by a research grant from the Max Kade Foundation. L.C.C. supported in part by a grant from the National Cancer Institute. Address correspondence to R.W.P., Department of Radiology, University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria (e-mail: rupert.prokesch@univie.ac.at).

	ABSTRACT

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PURPOSE: To assess the frequency of isoattenuating pancreatic adenocarcinoma with multi–detector row computed tomography (CT) and determine whether there are specific secondary signs that aid in detection.

MATERIALS AND METHODS: Fifty-three patients with pancreatic adenocarcinoma underwent contrast material–enhanced biphasic multi–detector row CT with curved planar reformation. Tumors were initially deemed isoattenuating or hypoattenuating to normal pancreatic parenchyma on the basis of visual inspection, and the degree of attenuation was confirmed by calculating the mean attenuation differences between normal pancreatic parenchyma and tumor (tumor-pancreas contrast) during the pancreatic phase. Indirect signs of pancreatic tumor were tabulated in patients with an isoattenuating tumor.

RESULTS: Of the 53 patients, six (11%) had isoattenuating tumors with a mean tumor-pancreas contrast of 9.25 HU ± 11.3 during the pancreatic phase and 4.15 HU ± 8.5 during the portal venous phase. The secondary signs of pancreatic tumor in these six patients included an interrupted pancreatic duct (n = 5), dilated biliary and pancreatic ducts (n = 1), atrophic distal pancreatic parenchyma (n = 3), and mass effect and/or convex contour abnormality (n = 3). The mean tumor-pancreas contrast for the remaining 47 patients was 74.76 HU ± 35.61 during the pancreatic phase.

CONCLUSION: With no visible tumor-pancreas contrast for isoattenuating tumors, indirect signs such as mass effect, atrophic distal parenchyma, and an interrupted duct sign are important indicators for the presence of tumor.

© RSNA, 2002

Index terms: Adenocarcinoma, 77.321 • Computed tomography (CT), multi–detector row, 77.12119 • Pancreas, neoplasms, 77.32

	INTRODUCTION

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With single-section helical computed tomography (CT), several authors have emphasized the value of a rapid-bolus biphasic technique for the local staging of pancreatic carcinoma (1–9). Specifically, imaging during a late arterial phase (ie, pancreatic phase) has been noted to improve the tumor conspicuity when compared with normal pancreas (4,8). The recent introduction of multi–detector row CT affords unprecedented scan acquisition speed, which enables the routine use of thin collimation to improve spatial resolution. We have recently noted, however, that even when high-resolution multi–detector row CT is performed in the pancreatic phase, some pancreatic carcinomas show remarkably little attenuation difference compared with the normal pancreas and may be considered isoattenuating. The purpose of this study was to assess the frequency of isoattenuating pancreatic adenocarcinoma with multi–detector row CT and determine whether there are specific secondary signs that aid in its detection.

	MATERIALS AND METHODS

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Patients
Between November 1998 and April 2001, 136 patients referred to our department in whom the presence of a pancreatic mass was suspected or known underwent multi–detector row CT. Pancreatic adenocarcinoma was diagnosed in 53 of the 136 patients (24 men aged 42–81 years [mean age, 58.2 years] and 29 women aged 43–79 years [mean age, 60.3 years]). A final diagnosis was achieved with biopsy in 13 patients, surgery in 17, and clinical follow-up in 23 (autopsy, n = 4; biopsy of metastases, n = 19). These 53 patients form the cohort of this study. The remaining 83 patients had signs of pancreatitis (n = 51, two had surgical confirmation), normal pancreas (n = 22), or diseases that did not involve the pancreas (n = 10). These diagnoses were based on CT and clinical findings.

All patients were referred for examination with a specific pancreatic protocol owing to some degree of clinical suspicion of pancreatic carcinoma. In addition, some patients were referred after conventional transverse CT or single–detector row spiral CT demonstrated no definitive mass because there remained a high clinical suspicion of a tumor. According to the institutional guidelines, review board approval was obtained for retrospective review of images on which the patient identity could be recognized. In addition, all patients who undergo CT at our institution give informed consent that their images may be used for research purposes.

CT Examination
CT scans were obtained with a multi–detector row CT scanner (LightSpeed QX/i; GE Medical Systems, Milwaukee, Wis) according to a dual-phase pancreatic protocol. Immediately before scanning, the patient was asked to ingest 900–1,000 mL of water as a negative intraluminal contrast material. An initial unenhanced localizer scan was obtained during a 10–12-second breath hold (10-mm collimation, pitch of 6 [high-speed mode], with low milliamperage [80 mA], and 120 kVp). A helical scan was then obtained that extended from 2 cm above the origin of the celiac trunk to 3 cm below the caudal extent of the pancreas. We used a small field of view (25 cm), which was centered over the superior mesenteric artery. After an 18- or 20-gauge catheter was placed in an antecubital vein, 140 mL of nonionic contrast material with an iodine content of 300 mg/mL (iohexol, Omnipaque; Nycomed-Amersham, Princeton, NJ) was injected at a rate of 4 mL/sec by using a power injector (Envision; Medrad, Indianola, Pa).

The scanning parameters were as follows: 120 kVp, 200–240 mA, 4 x 1.25-mm collimation, rotation time of 0.8 second, pitch of 6 (high-speed mode), and scanning delay of 40 seconds (pancreatic phase). A subsequent portal venous phase scan was obtained from the diaphragm to the symphysis pubis after a scanning delay of 70 seconds. Scanning parameters for this image included 120 kVp, 200–240 mA, 4 x 5-mm collimation, rotation time of 0.8 second, and pitch of six (high-speed mode). The matrix size was 512 x 512 in both series. The images obtained during the pancreatic phase were reconstructed at 0.5- and 5-mm intervals in the portal venous phase. These data were then transferred to an independent workstation, and curved planar reformations of the pancreas were generated from pancreatic phase images in all 53 patients.

Image Analysis
Mean CT attenuation values of tumor and pancreas were obtained from the pancreatic phase images by means of region-of-interest (ROI) analysis performed by two readers; decisions were made with consensus. As large an area as possible was included in the ROI for both tumor and normal pancreas. Care was taken to exclude macroscopic enhanced blood vessels and pancreatic duct from the ROI. For ROI measurements, the tumor was assumed to be located immediately adjacent to the obstructed pancreatic duct.

The difference between the attenuation of tumor and pancreas (tumor-pancreas contrast) was calculated for each patient. By convention, we chose to report these contrast differences as absolute values, or positive numbers, in each case. The mean enhancement of normal pancreatic parenchyma was calculated as the difference between the pancreatic attenuation on pancreatic phase and precontrast images.

In addition, mean CT attenuation values of tumor and normal pancreatic parenchyma were also obtained from portal venous phase images for cases deemed isoattenuating at visual inspection. The tumor-pancreas contrast during the portal venous phase was calculated for these cases in the same fashion. All attenuation values were calculated from transverse images.

Of the 53 patients in the study, six were categorized as having visually isoattenuating tumors. In these patients, the presence and location of a pancreatic mass was inferred from secondary signs such as obstruction of the pancreatic duct and mass effect. Conversely, the remaining 47 patients had masses that were readily appreciated as differing in attenuation from normal pancreatic parenchyma.

Transverse images and curved planar reformations were analyzed for indirect signs of tumor, such as interrupted pancreatic duct, dilated pancreatic and/or biliary duct, mass effect and/or contour abnormality, and atrophic distal pancreatic parenchyma.

Statistical Analysis
A nonparametric Mann-Whitney U test was used to test the hypothesis that the CT attenuation in the two groups (patients with hypoattenuating tumors [n = 46] and patients with isoattenuating tumors [n = 6]) are identical. The alternative hypothesis was that the populations are different and that the patients with hypoattenuating tumors have higher Hounsfield units.

A Wilcoxon signed-rank test was used to assess Hounsfield unit differences between isoattenuating tumors and normal pancreatic parenchyma. The null hypothesis was that the distribution of differences between pairs of measurements (n = 6) is symmetric around zero. The alternative hypothesis was that the differences tend to be smaller or larger than zero. For both tests, differences with a P value of less than .05 were considered statistically significant.

	RESULTS

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Of the 53 patients, six (11%) had tumors that were considered to be visually isoattenuating. The mean attenuation difference between normal pancreas and tumor for these six patients was 9.25 HU ± 11.3 (mean ± SD) during the pancreatic phase and 4.15 HU ± 8.5 during the portal venous phase. Conversely, the mean attenuation difference between normal pancreas and tumor for the remaining cases was 74.76 HU ± 35.61 during the pancreatic phase. The mean enhancement of normal pancreatic parenchyma during pancreatic phase imaging was 93.6 HU ± 27.9. In all 53 cases, tumors were either visually hypoattenuating or visually isoattenuating in both the pancreatic and portal venous phases. Results of the Mann-Whitney U test revealed a significant difference between the two groups of tumors in the pancreatic phase (P < .001) (Fig 1). For patients with isoattenuating tumors, results of the Wilcoxon signed-rank test showed that the Hounsfield units in neither the pancreatic (P = .34) nor portal venous (P = .58) phases were significantly different from that of normal pancreatic tissue.

View larger version (18K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Box and whisker graph shows the mean tumor-pancreas contrast for isoattenuating and hypoattenuating tumors in the pancreatic phase.

View larger version (147K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Images in a 62-year-old man with pathologically proved adenocarcinoma of the pancreatic head. (a, b) Transverse contrast material-enhanced CT scans obtained in the pancreatic phase demonstrate an ill-defined mass (* in a) that abuts both the gastroduodenal artery (arrow in a) and the medial wall of the duodenum. (c) Curved planar reformation of the pancreas shows a dilated distal pancreatic duct (arrows) that terminates at an ill-defined isoattenuating mass (*).

View larger version (149K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Images in a 62-year-old man with pathologically proved adenocarcinoma of the pancreatic head. (a, b) Transverse contrast material-enhanced CT scans obtained in the pancreatic phase demonstrate an ill-defined mass (* in a) that abuts both the gastroduodenal artery (arrow in a) and the medial wall of the duodenum. (c) Curved planar reformation of the pancreas shows a dilated distal pancreatic duct (arrows) that terminates at an ill-defined isoattenuating mass (*).

View larger version (150K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Images in a 62-year-old man with pathologically proved adenocarcinoma of the pancreatic head. (a, b) Transverse contrast material-enhanced CT scans obtained in the pancreatic phase demonstrate an ill-defined mass (* in a) that abuts both the gastroduodenal artery (arrow in a) and the medial wall of the duodenum. (c) Curved planar reformation of the pancreas shows a dilated distal pancreatic duct (arrows) that terminates at an ill-defined isoattenuating mass (*).

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Images in a 64-year-old woman with pathologically proved adenocarcinoma of the pancreas. (a) Transverse contrast-enhanced CT scan obtained in the pancreatic phase demonstrates an isoattenuating mass (*) in the body of the pancreas. A dilated distal pancreatic duct (left arrow) and distal pancreatic atrophy (right arrow) are seen. (b) Curved planar reformation of the pancreas shows distal pancreatic atrophy (arrow) and a dilated distal pancreatic duct terminating at an ill-defined isoattenuating mass (*).

View larger version (147K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Images in a 64-year-old woman with pathologically proved adenocarcinoma of the pancreas. (a) Transverse contrast-enhanced CT scan obtained in the pancreatic phase demonstrates an isoattenuating mass (*) in the body of the pancreas. A dilated distal pancreatic duct (left arrow) and distal pancreatic atrophy (right arrow) are seen. (b) Curved planar reformation of the pancreas shows distal pancreatic atrophy (arrow) and a dilated distal pancreatic duct terminating at an ill-defined isoattenuating mass (*).

	DISCUSSION

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Despite developments in magnetic resonance imaging and endoscopic ultrasonography, CT remains the modality used most frequently for the detection and staging of pancreatic carcinoma. Dynamic CT has a reported sensitivity of as high as 97% in the detection of pancreatic cancer, accuracy of staging as high as 93%, and positive predictive values for surgical unresectability between 89% and 100% (2,3). By implementing two-phase helical CT with scanning during both the pancreatic and hepatic phases, Lu et al (4) reported a significantly greater mean tumor-pancreas contrast during the pancreatic phase. Their technique helps optimize the detectability of pancreatic adenocarcinoma, which tends to enhance less than the surrounding parenchyma on pancreatic phase images.

In our cohort of 53 patients, however, six (11%) had tumors that were visually isoattenuating to normal pancreatic parenchyma at both pancreatic and portal venous phase imaging. This finding suggests that a substantial number of pancreatic tumors in the general population may present a challenge for detection, despite the use of optimal scanning parameters. The clinical relevance of this finding is substantial, given that early detection represents the only chance for cure in most cases of pancreatic cancer. To our knowledge, this finding has not been previously reported in the literature.

The mean tumor-pancreas contrast in the cases deemed isoattenuating at visual inspection—9.25 HU on pancreatic phase images and 4.15 HU on portal venous phase images—is consistent with previously reported data that suggest a difference of at least 10–15 HU is necessary for visual detection (10). In addition, the mean enhancement of normal pancreatic parenchyma during the pancreatic phase was 93.6 HU, whereas that reported by Hollett et al (11) with single–detector row helical CT was 82 HU.

To ensure that such cases of isoattenuating pancreatic tumors do not go undetected, it is imperative that interpretation of these images include evaluation for ancillary signs of pancreatic tumor. In our cohort of six patients, five had a distal pancreatic duct that was dilated up to the site of the tumor, the so-called interrupted duct sign. In addition to review of the transverse images, curved planar reformations clearly depicted the obstructed ductal system in all patients: Three patients had atrophy of the pancreatic parenchyma distal to the mass and three had a clear convex contour deformity of the pancreatic parenchyma at the level of the mass. A potential pitfall in use of this finding alone to make the diagnosis of a possible isoattenuating pancreatic mass results from the anatomic variability of the pancreas, particularly in the region of the head. Ross et al (12) described three types of pancreatic head lobulations, which represent normal variation in anatomy. A scenario can be envisioned in which an isoattenuating mass in the pancreatic head could mimic a normal lobulation or vice versa.

Clearly, without the use of attenuation differences to help define the presence of a pancreatic mass, morphologic features must be depended on to help identify a visually isoattenuating tumor. Three-dimensional reconstructions such as curved planar reformations can be invaluable for depicting the pancreas along its longitudinal axis; this capability facilitates identification of such morphologic abnormalities (13,14). For example, when the entire length of obstructed duct is seen on one image (Fig 2c), the interrupted duct sign becomes easier to identify and the point of obstruction becomes obvious. In fact, this may be the single most important sign of a visually isoattenuating pancreatic mass because a dilated pancreatic duct was identified in all six of our cases of visually isoattenuating tumors. Nino-Murcia et al (13) and Fishman et al (15) recently described the use of three-dimensional reformations in the evaluation of pancreatic tumors; they pointed out that these reformations can distill the pertinent anatomic information from hundreds of transverse source images obtained with multi–detector row CT into a few key images.

Limitations of our study include the small number of cases of visually isoattenuating pancreatic tumors. Even with this small population, however, several secondary signs—such as the interrupted duct sign—appeared to be reliable indicators of the presence of a mass, even in the absence of a clear attenuation difference. Specifically, the combined presence of the interrupted duct sign with mass effect should arouse suspicion of a pancreatic tumor rather than a benign stricture. Because of the small number of patients with isoattenuating tumors, we did not compare the frequency of secondary signs of pancreatic tumor in patients with isoattenuating and hypoattenuating tumors. Obstruction of the pancreatic duct is not specific for pancreatic carcinoma and is also seen in focal pancreatic inflammatory masses. An additional difficulty that was encountered during this study was the determination of exactly where to measure attenuation values in the ROIs of visually isoattenuating tumors (owing to their lack of conspicuity). For ROI measurement, however, the tumor was assumed to be located immediately adjacent to the obstructed pancreatic duct.

The relatively high frequency (11%) of isoattenuating tumors was somewhat surprising to us, but we do not have enough information to determine whether this is the proportion that would be expected in a broader population. In some of our patients, multi–detector row CT was performed after initial CT scans demonstrated a dilated pancreatic duct but no definitive mass, thereby leading to selection bias. Although we do not expect that a change in the contrast material injection protocol would affect the depiction of isoattenuating lesions, we do believe that the ability to perform high-quality multiplanar reformations with multi–detector row CT is an advantage that may allow diagnosis of otherwise subtle lesions. With regard to the biologic basis of isoattenuating tumors, at this point we can only speculate that the observed variability in enhancement reflects intrinsic variations in tumor vascularity.

In conclusion, although the conspicuity of most pancreatic tumors can be optimized with current biphasic multi–detector row CT protocols, a substantial number of tumors are visually isoattenuating to pancreatic parenchyma on both pancreatic and portal venous phase images. With no visible tumor-pancreas contrast, indirect signs such as mass effect, atrophic distal parenchyma, and an interrupted duct sign are important indicators of the presence of tumor. In our experience, curved planar reformation is a useful tool for depicting the secondary signs for such pancreatic tumors, which may be the only clues to their presence.

	FOOTNOTES

 
Abbreviation: ROI = region of interest

Author contributions: Guarantors of integrity of entire study, R.B.J., R.W.P.; study concepts, C.F.B., R.B.J., R.W.P.; study design, R.W.P., L.C.C.; literature research, R.B., R.W.P.; clinical studies, L.C.C., R.B.J., C.F.B.; data acquisition, L.C.C., C.F.B., R.B.J.; data analysis/interpretation, all authors; statistical analysis, R.B., R.W.P.; manuscript preparation, R.W.P., L.C.C.; manuscript definition of intellectual content, R.B.J., C.F.B.; manuscript editing, R.B.J., L.C.; manuscript revision/review, C.F.B., R.B., R.B.J.; manuscript final version approval, R.B.J., C.F.B.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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6. O’Malley ME, Boland GW, Wood BJ, Fernandez-Del-Castillo C, Warshaw AL, Mueller PR. Adenocarcinoma of the head of the pancreas: determination of surgical unresectability with thin section pancreatic-phase CT. AJR Am J Roentgenol 1999; 173:1513-1518.[Abstract]
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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2243011284v1 224/3/764    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Prokesch, R. W. Articles by Jeffrey, R. B. Search for Related Content PubMed PubMed Citation Articles by Prokesch, R. W. Articles by Jeffrey, R. B., Jr