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Salivary Gland Tumors: Evaluation with Two-Phase Helical CT¹

¹ From the Department of Radiology, College of Medicine, Dongguk University, Pohang Hospital, Kyungsangbuk-Do, Korea (D.S.C., H.K.L.); and the Departments of Radiology (D.G.N., H.S.B., C.K.K., J.M.C.) and Pathology (Y.H.K.), College of Medicine, Sungkyunkwan University, Samsung Medical Center, 50 Irwon-Dong, Kangnam-Ku, Seoul 135-710, Korea. Received August 11, 1998; revision requested October 5; final revision received February 24, 1999; accepted July 27. Address reprint requests to D.G.N. (e-mail: dgna@smc.samsung.co.kr).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate two-phase helical computed tomography (CT) in the characterization of salivary gland tumors.

MATERIALS AND METHODS: Sixty-four patients with major salivary gland tumors underwent two-phase helical CT. The histopathologic diagnosis was obtained by means of surgical resection or biopsy in all patients. After the injection of 90 mL of contrast material at a rate of 3 mL/sec, helical CT scans were obtained at early and delayed phases with scanning delays of 30 and 120 seconds, respectively. The attenuation change and enhancement patterns in the tumors were assessed. The attenuation change in the tumor also was assessed quantitatively as the ratio of the CT number (in Hounsfield units) at delayed phase scanning to that at early phase scanning.

RESULTS: There were 35 pleomorphic adenomas, nine Warthin tumors, and 20 malignant tumors. Two-phase helical CT showed increase in attenuation in 30 (86%) pleomorphic adenomas, decrease in eight (89%) Warthin tumors, and increase in 11 (55%) and no change in eight (40%) malignant tumors at delayed phase scanning. A multinodular enhancement pattern was found in only 12 (34%) pleomorphic adenomas. The ratio of CT numbers was significantly different between Warthin tumors and pleomorphic adenomas and between Warthin tumors and malignant tumors.

CONCLUSION: The analysis of enhancement patterns by using two-phase helical CT will be helpful in the differential diagnosis of salivary gland tumors.

Index terms: Computed tomography (CT), helical, 264.12114, 264.12115 • Salivary glands, CT, 264.12112, 264.12113, 264.12114, 264.12115 • Salivary glands, neoplasms, 264.36, 264.37

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Computed tomography (CT) has been widely used for the evaluation of salivary gland tumors and is useful for the detection of the tumor and the assessment of tumor extent (1–8). However, there is a limitation in the CT prediction of the histopathologic characteristics of tumors. Although CT findings of irregular tumor margin and infiltration into adjacent structures suggest malignancy, a malignant tumor may mimic a benign tumor on CT scans. There are also considerable overlaps of CT features among benign salivary gland tumors on CT scans (2,4–6).

The introduction of helical CT recently has increased the usefulness of CT as an imaging method for the detection and characterization of tumors in areas other than the salivary gland, such as the liver (9,10). However, to our knowledge, there is no report of the use of helical CT for characterization of salivary gland tumors.

The purpose of this study was to perform two-phase dynamic helical CT in patients with salivary gland tumors and to describe the enhancement characteristics of the tumors.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Sixty-four patients (31 male patients, 33 female patients; age range, 15–82 years; mean age, 49 years) were referred for evaluation of major salivary gland masses with use of two-phase helical CT. Of 64 patients, 53 had parotid gland tumors and 11 had submandibular gland tumors. The histopathologic diagnosis was confirmed at surgical resection (n = 62) or open biopsy (n = 2) in all patients.

All examinations were performed with helical CT scanners (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). A total of 90 mL of iopamidol (Iopamiro 300; Bracco, Milan, Italy) was administered into an antecubital vein at a rate of 3 mL/sec by using a power injector. Early and delayed phase scans were then obtained with scanning delays of 30 and 120 seconds, respectively. Scanning began at the skull base and continued toward the thoracic inlet level with the following parameters: 35-second acquisition time, 5-mm collimation, and 5 mm/sec table speed. From the volumetric data, contiguous transverse images were reconstructed at 5-mm intervals. Thirty-five sections were obtained at each phase. In 52 patients (32 with pleomorphic adenomas, four with Warthin tumors, and 16 with malignant tumors), coronal images also were obtained 6–25 minutes (mean, 12 minutes) after the initiation of contrast material injection.

Initially, each CT scan was evaluated independently by two radiologists (D.S.C., D.G.N.) who were unaware of the result of histopathologic diagnosis, and they reached a consensus when there was a discrepancy in the interpretation of the CT images. First, visual assessment of the enhancement patterns of tumors was performed. The attenuation change in the tumor between early and delayed phases was analyzed, and it was categorized as "decrease," "no change," or "increase." When a tumor showed more than two types of attenuation change within one mass, it was categorized as "mixed." An obvious cystic or necrotic area that showed constant low attenuation at each phase was excluded from the assessment of attenuation change. The enhancement of the tumors also was assessed at each phase and classified as homogeneous, heterogeneous with intratumoral low attenuation, or multinodular. The visual assessment of CT images at each phase was performed at the same window width (240 HU) and level (20 HU) in all patients.

Second, we quantitatively measured the CT numbers (in Hounsfield units) of the tumors at each phase by means of circular regions of interest. The region-of-interest circle was made as large as possible (8–30 mm²), and obvious cystic or necrotic areas were excluded. The ratio of the tumoral CT number at delayed phase scanning to that at early phase scanning also was calculated.

Analysis of variance, or ANOVA, was used for the statistical analysis of differences in the tumoral CT numbers at each phase and in the ratio of the tumoral CT numbers at delayed phase scanning compared with those at early phase scanning among pleomorphic adenomas, Warthin tumors, and malignant tumors.

	RESULTS

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The results are summarized in the Table. There were 35 pleomorphic adenomas, nine Warthin tumors, and 20 malignant tumors: three mucoepidermoid carcinomas, six adenoid cystic carcinomas, three carcinoma ex pleomorphic adenomas, three ductal carcinomas, one myoepithelial carcinoma, one sebaceous carcinoma, and three lymphomas. The maximum transverse diameters of the tumors were 12–170 mm (mean, 34 mm), and there was no statistically significant difference among the histopathologic types of the tumors (P > .05, analysis of variance).

View larger version (141K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Pleomorphic adenoma in the parotid gland in a 29-year-old woman. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the superficial lobe of the right parotid gland. There is mild enhancement of the tumor. (b) Transverse delayed phase scan shows homogeneous and strong enhancement of the tumor (arrows).

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Pleomorphic adenoma in the parotid gland in a 29-year-old woman. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the superficial lobe of the right parotid gland. There is mild enhancement of the tumor. (b) Transverse delayed phase scan shows homogeneous and strong enhancement of the tumor (arrows).

View larger version (142K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Pleomorphic adenoma in the submandibular gland in a 17-year-old adolescent boy. (a) Transverse early phase helical CT scan shows a round mass (arrows) in the left submandibular gland. This mass shows slightly decreased attenuation compared with that of muscle. (b) Transverse delayed phase image demonstrates slight enhancement of the mass (arrows).

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Pleomorphic adenoma in the submandibular gland in a 17-year-old adolescent boy. (a) Transverse early phase helical CT scan shows a round mass (arrows) in the left submandibular gland. This mass shows slightly decreased attenuation compared with that of muscle. (b) Transverse delayed phase image demonstrates slight enhancement of the mass (arrows).

View larger version (152K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Warthin tumor in the parotid gland in a 45-year-old man. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the left parotid gland. There is strong enhancement of the tumor with central low attenuation suggestive of a cystic or necrotic area. (b) Transverse delayed phase scan shows decreased enhancement of the tumor (arrows).

View larger version (152K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Warthin tumor in the parotid gland in a 45-year-old man. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the left parotid gland. There is strong enhancement of the tumor with central low attenuation suggestive of a cystic or necrotic area. (b) Transverse delayed phase scan shows decreased enhancement of the tumor (arrows).

View larger version (141K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Mucoepidermoid carcinoma in the parotid gland in a 44-year-old woman. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the left parotid gland. There is heterogeneous low attenuation in the center of the mass. (b) Transverse delayed phase image shows no substantial change in attenuation and heterogeneity of the mass (arrows).

View larger version (143K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Mucoepidermoid carcinoma in the parotid gland in a 44-year-old woman. (a) Transverse early phase helical CT scan shows a well-defined mass (arrows) in the left parotid gland. There is heterogeneous low attenuation in the center of the mass. (b) Transverse delayed phase image shows no substantial change in attenuation and heterogeneity of the mass (arrows).

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 5a. Pleomorphic adenoma in the parotid gland in a 32-year-old woman. (a) Transverse early phase helical CT scan shows multinodular heterogeneous enhancement of the mass. The central portion (short arrows) of the mass is more strongly enhanced than is the peripheral area (long arrow) of the mass. (b) Transverse delayed phase CT scan shows slightly increased enhancement of the two parts of the tumor, which are labeled as in a. (c) Coronal image obtained 7 minutes after contrast material injection shows that the multinodular enhancement of the tumor (arrows) has disappeared and become homogeneous.

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 5b. Pleomorphic adenoma in the parotid gland in a 32-year-old woman. (a) Transverse early phase helical CT scan shows multinodular heterogeneous enhancement of the mass. The central portion (short arrows) of the mass is more strongly enhanced than is the peripheral area (long arrow) of the mass. (b) Transverse delayed phase CT scan shows slightly increased enhancement of the two parts of the tumor, which are labeled as in a. (c) Coronal image obtained 7 minutes after contrast material injection shows that the multinodular enhancement of the tumor (arrows) has disappeared and become homogeneous.

View larger version (153K): [in this window] [in a new window] [Download PPT slide]   Figure 5c. Pleomorphic adenoma in the parotid gland in a 32-year-old woman. (a) Transverse early phase helical CT scan shows multinodular heterogeneous enhancement of the mass. The central portion (short arrows) of the mass is more strongly enhanced than is the peripheral area (long arrow) of the mass. (b) Transverse delayed phase CT scan shows slightly increased enhancement of the two parts of the tumor, which are labeled as in a. (c) Coronal image obtained 7 minutes after contrast material injection shows that the multinodular enhancement of the tumor (arrows) has disappeared and become homogeneous.

The ratio of tumoral CT numbers at delayed phase scanning to those at early phase scanning was 1.33 ± 0.24 for pleomorphic adenomas, 0.82 ± 0.15 for Warthin tumors, and 1.16 ± 0.22 for malignant tumors. There were significant differences in the ratio of CT numbers between Warthin tumors and pleomorphic adenomas (P = .000, analysis of variance) and between Warthin tumors and malignant tumors (P = .001, analysis of variance). However, no significant difference in the ratio was found between pleomorphic adenomas and malignant tumors (P = .10, analysis of variance). Compared with delayed phase scans, coronal scans showed no change in the mean tumoral CT number in pleomorphic adenomas and decrease in malignant and Warthin tumors (Fig 6).

View larger version (16K): [in this window] [in a new window] [Download PPT slide]   Figure 6. Time-attenuation curves for pleomorphic adenomas (n = 35), Warthin tumors (n = 9), and malignant tumors (n = 20). Pleomorphic adenomas and malignant tumors show increased attenuation at delayed phase scanning. Between delayed phase and coronal scanning, pleomorphic adenomas show no change in attenuation, but malignant tumors show mild decrease in attenuation. The attenuation of Warthin tumors progressively decreases from early phase to coronal scanning. Error bars indicate SDs.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

The enhancement patterns of tumors are influenced by many biologic factors. These include vascularity (size and number of vessels, histopathologic character of neovessels, arteriovenous architecture of neovessels), histopathologic cell types, and histologic components of the tumors. Scanning parameters also influence the enhancement patterns of tumors (12–14). In our study of two-phase helical CT of salivary gland tumors, the attenuation change between early and delayed phase scans was clearly different between Warthin tumors and pleomorphic adenomas and between Warthin tumors and malignant tumors in most cases. Different histologic components of tumor cells and different architecture of tumoral neovascularity may cause these different enhancement patterns of the tumors. Warthin tumor consists of an epithelial, monomorphic, mostly oncocytic component and a lymphoid stroma (15,16). Pleomorphic adenoma, as the term indicates, contains diverse histologic components of epithelial and stromal elements. In epithelial differentiation, it can contain duct epithelium, myoepithelial cells, epidermoid cells, and other cell forms. The stroma can show mucoid, chondroid, mucoid-chondroid, fascicular, and hyalin-fibrous differentiation. Morphologic diversity can be evident among different tumors and within the same lesion (15,16).

The results of our study showed a pattern of delayed enhancement in pleomorphic adenoma and a pattern of strong enhancement at early phase scanning with a decrease at delayed phase scanning in Warthin tumor. Although the mechanism of contrast enhancement on magnetic resonance (MR) images is not identical to that on CT scans, our results were consistent with those of Takashima et al (17) who evaluated head and neck lesions by using dynamic MR imaging. They reported that dynamic MR imaging showed peak signal intensity at 0–30 seconds after the injection of a bolus of contrast material in Warthin tumor and showed peak signal intensity at 30–210 seconds or gradual increase in signal intensity for up to 5 minutes in pleomorphic adenoma and malignant tumor.

In our study, although 11 (55%) of 20 malignant tumors also showed increase in enhancement at delayed phase scanning similar to that of pleomorphic adenoma, a mixed pattern of attenuation change between early and delayed phase scanning and multinodular enhancement were found only in pleomorphic adenomas. This complex enhancement of pleomorphic adenomas may be because of the diverse histologic components of a pleomorphic adenoma. In nine (75%) of 12 pleomorphic adenomas that showed multinodular heterogeneous enhancement on early phase scans, the multinodular enhancement became homogeneous on delayed phase scans (n = 1) or coronal scans (n = 8). This change in enhancement in pleomorphic adenoma on coronal scans suggests that pleomorphic adenomas can show homogeneous enhancement more on conventional CT scans obtained at a late time after the infusion of contrast material than on two-phase helical CT scans. Although multinodular enhancement was found in only 34% of pleomorphic adenomas, this, when present, may be highly suggestive of pleomorphic adenoma.

Warthin tumor has a greater tendency to undergo gross cystic change than any of the other salivary gland tumors, whereas many malignant tumors contain necrotic areas (18). These cystic or necrotic areas are seen as focal intratumoral low attenuation on CT scans (Fig 3). In most of the Warthin and malignant tumors that showed intratumoral low attenuation on early phase scans, the portion of intratumoral low attenuation showed no substantial change in attenuation on delayed phase and coronal scans (Fig 4). However, in some of the pleomorphic adenomas that showed intratumoral low attenuation on early phase scans, the portion of lower attenuation showed progressive increase in attenuation on delayed phase and coronal scans. Therefore, the focal intratumoral low attenuation in pleomorphic adenoma on early phase helical CT scans may suggest a solid portion and a cystic or necrotic area.

Various kinds of malignant tumors can develop in the major salivary glands. In our study, seven kinds of malignant tumors were included. All malignant lymphomas and five (83%) of six adenoid cystic carcinomas showed homogeneous enhancement, whereas all mucoepidermoid carcinomas, carcinoma ex pleomorphic adenomas, and ductal carcinomas showed heterogeneous enhancement with intratumoral low attenuation. However, except for ductal carcinomas that showed increased enhancement on delayed phase scans, the attenuation change in the tumors between early and delayed phases was variable within the same histopathologic type, as well as among different histopathologic types of tumors.

Accurate preoperative prediction of the histopathologic characteristics of the tumors with imaging findings is useful for adequate surgical planning and for the prediction of tumor prognosis. However, there is a limitation in the characterization of the salivary gland tumors with conventional CT. This study may provide useful criteria for the characterization of salivary gland tumors.

This study has a limitation in that the two-phase helical CT technique could not provide compact data for the analysis of time-attenuation curves of tumoral enhancement that could be useful for the complete assessment of the enhancement patterns of tumors. In addition, the variable scanning times of the coronal scans in our study also limit the accurate assessment of tumoral enhancement at the late phase after contrast material injection.

In conclusion, two-phase helical CT showed a pattern of delayed enhancement in pleomorphic adenoma and a pattern of strong enhancement at early phase scanning with a decrease at delayed phase scanning in Warthin tumor. Although increase in enhancement at delayed phase scanning also was found in malignant tumor, multinodular enhancement might be highly suggestive of pleomorphic adenoma. The evaluation of enhancement patterns at two-phase helical CT will be helpful in the differential diagnosis of salivary gland tumors.

	Acknowledgments

 
We thank Dongwan Cho, PhD, for his careful review of the manuscript.

	Footnotes

 
Author contributions: Guarantor of integrity of entire study, D.G.N.; study concepts and design, D.S.C., D.G.N.; definition of intellectual content, D.S.C., D.G.N.; literature research, D.S.C.; clinical studies, D.S.C., D.G.N., C.K.K., J.M.C.; data acquisition, D.S.C., D.G.N.; data analysis, D.S.C., D.G.N., H.S.B., Y.H.K.; statistical analysis, D.S.C.; manuscript preparation, D.S.C.; manuscript editing, D.G.N.; manuscript review, D.G.N., H.K.L.

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