MR Imaging Features of Basal Cell Adenoma of the Parotid Gland : Differentiation from Pleomorphic Adenoma and Warthin Tumor

Citation: Ming-Wei X, Zi-Liang C, Hai-Yan W, Guang-Zi S, Hui-Jun H, et al. (2018) MR Imaging Features of Basal Cell Adenoma of the Parotid Gland: Differentiation from Pleomorphic Adenoma and Warthin Tumor. Int J Radiol Imaging Technol 4:033. doi.org/10.23937/2572-3235.1510033 Received: January 12, 2018: Accepted: May 02, 2018: Published: May 04, 2018 Copyright: © 2018 Ming-Wei X, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Fine needle aspiration cytology (FNAC) is a preoperatively diagnostic choice.Whereas FNAC could lead to a risk of possible spread of tumor cells, which can elevate the likelihood of local recurrence [7].To date, CT or MR imaging has become a routine preoperative workup for the diagnosis of parotid gland tumors.
CT imaging features of BCA, PA and WT had been well described.For example, BCA is featured as intratumor cystic areas, linear bands or stellate-shaped non-enhanced areas [8].PA manifests as multinodular enhancement on the early-phase and increased enhancement on the delayed phase on dynamic contrast-enhanced CT [9,10].WT shows a pattern of strong enhancement on the early phase but decreased enhancement on the delayed phase [9,11].Two types of enhancement patterns BCA were reported [12].So far, MR imaging has been increasingly used for the diagnosis of parotid tumors.Recently, several new MR tech-

Introduction
Basal cell Adenoma (BCA) is an uncommon, benign epithelial tumor of the parotid gland, accounting for approximately 1%-3% of all parotid gland benign tumors [1,2].Pleomorphic adenoma (PA) and Warthin tumor (WT) are the other two most popular benign parotid gland tumors.BCA is the third most common benign parotid tumors, following WT and PA.The incidence of BCA is far less than parotid PA and WT, but the main clinical presentations of BCA such as slow-growing, asymptomatic painless mass, and well-defined cystic or Check for updates and communication systems (Centricity RIS CE 3.0; GE Healthcare, Milwaukee, WI, USA) by two experienced radiologists in consensus and in a blinded manner (Z.W, with 15 years of experience with diagnostic imaging, and M.W.X, with 8 years of experience with diagnostic imaging).MR imaging features including the number of tumors (solitary or multifocal), location, size, shape, capsule, signal intensity, intratumor cystic area and contrast enhancement pattern were determined.Tumor location was divided into superficial and deep parotid lobes on the right or left sides.Tumor size was measured in maximal dimension on the transverse plane.The shape of the lesion was classified as regular (round/ovoid) or lobulated.The signal intensity (SI) was assessed only for the solid portion of tumors.Tumor SIs were classified as hyperintense, hypointense and mixed hyper-and hypo-intense on T2 weighted images, and as hypointense and mixed hyper-and hypo-intense on T1 weighted images compared with the surrounding uninvolved parotid gland.Tumor enhancement was assessed on the fat-suppressed contrast-enhanced T1 weighted images.The degrees of enhancement were graded as mild (less or equal to the surrounding parotid tissues) and marked (higher than the parotid gland).The presence of unenhanced cystic area was recorded, and their patterns were categorized as round/ovoid or irregular, and the irregular unenhanced area represents a branched or strip shape.The presence of capsule was assessed.

Statistical analysis
Data was presented as a mean ± standard deviation and n (%).MR imaging features of the number of tumors (solitary or multifocal), location (left/right side or superficial/deep lobe), shape, capsule, signal intensity, intratumor cystic area and contrast enhancement were compared between BCA and PA/WT.The categorical variables were analyzed by using continuity corrected Chi-square test or Fisher's exact test.The size and patient age were compared by Mann-Whitney U test.All statistical tests were performed by using software (SPSS, version 17.0, Chicago, IL, USA).P-values < 0.05 were considered to indicate statistical significance.

Characteristics of patients
The mean age of patients with BCAs was significantly greater than that in PAs (mean age ± SD 59.6 ± 8.7 versus 39.8 ± 14.5 years, P < 0.001).No significant difference was found in sex distribution between BCAs and PAs or WTs (P < 0.474) (Table 1).Three PA patients had two tumors.Ten WT patients had multiple tumors, including 2 in 5 patients, 4 in 4 patients and 5 in 1 patient.The number of lesions of BCAs, PAs and WTs were 9, 62 and 58, respectively (Table 1).

MR imaging features
The MR imaging features in BCAs, PAs and WTs are niques have been reported to be useful in diagnosis of parotid tumors, such as arterial spin labelling-based perfusion MR imaging and diffusion-weighted imaging [13,14].Because of the technique limitation and accompanied additional expenses, conventional MR imaging remains the mainstay of preoperative diagnostic means for parotid tumors.Previously, the clinicopathological features of BCA versus PA and WT have been described [2].However, unlike PA and WT, MR imaging features of BCA have not been well described.
In this study, we retrospectively analyzed the MR imaging findings in large series including 9 patients with BCA, 59 patients with PA and 37 patients with WT.The purpose of this study is to identify characteristic MR imaging features of BCAs, which can be helpful for the differentiation between BCAs and PAs or WTs.

Patients
Between January 2010 and March 2016, 105 patients with pathologically confirmed parotid benign tumors including BCA (n = 9), PA (n = 59) and WT (n = 37) in our hospital were enrolled.All patients underwent MR imaging before surgery.The study was approved by the institutional review board of our institution, and patient informed consent was waived for this type of review.There were 68 men and 37 women, aged from 14 years to 87 years with a mean of 49 years.All patients were treated with surgical resection.The medical records of all patients are well maintained.

MR Imaging
MR imaging was performed in 43 patients by using a 1.5-T MR scanner (Gyroscan Intera; Philips Medical Systems, Best, Netherlands) and in 62 patients by using a 3.0-T MR scanner (Achieva; Philips Medical Systems, Netherlands) with a head and neck synergy coil to allow for coverage from the skull base to the thoracic inlet.MR protocol consisted of plain scan including axial Fast Spin Echo (FSE) T1 and T2 weighted imaging and contrast-enhanced imaging.Axial T2 weighted imaging was acquired by using parameters as follows: TR/TE = 700/2.

Imaging analysis
All MR images were reviewed on a picture archiving was no significant difference with respect to the location, tumor size, and capsule among three types of tumors (P = 0.346-1.000)(Table 2).

Discussion
BCAs are the rare, benign epithelial tumor and lacks   accumulated microscopic cysts containing proteinous fluid with foamy cells, red cells, and neutrophils [11].
The marked enhancement of solid portion on the fat-suppressed contrast-enhanced T1 weighted images was found in all cases of BCAs in our study.However, in the study by Okahara, et al. such characteristic feature of marked enhancement has not been described [17].Unlike non-fat-suppressed contrast-enhanced T1 weighted imaging applied in most cases (7 of 8 patients) in their study [17], we used fat-suppressed T1-weighted images as regards fat tissue is a substantial component of the parenchyma of the parotid gland [22].Such marked enhancement on the fat-suppressed T1-weighted images is useful for the distinction BCA from WT, which is characterized by mild enhancement on the venous phase due to early enhancement and subsequent washout pattern on dynamic study [11].Lee, et al. reported that on CT imaging BCAs with large cystic areas showed gradual and additional enhancement on the delayed phase, and mostly solid-looking BCAs showed marked contrast enhancement on the early phase and a subsequent decrease on the delayed phase [11].In our study, we found both types of BCAs showed obvious enhancement on the contrast-enhanced T1 weighted imaging.This difference might be related to the distinc-the mesenchyme-like component that pleomorphic adenomas possess [15,16].Their CT, MR or ultrasound imaging features are characterized as a round, well-defined, obviously enhanced solid mass with or without a cystic portion [12,17,18].In this study, all BCAs had an ovoid shape, which is significantly different from PAs, as most of PAs (59.68%) showed lobulated contour.This might be caused by the different growth rates of different cell types within the tumor of PA.Moreover, PAs have abundant myxoid areas histologically and incomplete encapsulation, which can lead to a lobulated contour [19,20].
The hypointense signal of solid portion on T2 weighted imaging was observed in all cases of BCAs in our study.This finding is in consistence with that by Okahara, et al. [17].Benign PAs usually show bright signal intensity on T2 weighted images because of an area containing abundant fibromyxoid stroma [19,21].In our series, more than 80% of PAs had the area of high signal intensity on T2 weighted images.The lower signal intensity than surrounding normal parotid gland on T2 weighted images might be a useful feature for differentiating BCA from PA.This low signal intensity on T2 weighted images probably corresponds to the high cellularity.WT shows similar hypointense signal on T2 weighted images as BCA.Such hypointense signal was reported to be caused by the cellular components with  marked enhancement on the fat-suppressed T1-weighted imaging.PA is more likely to exhibit mixed hyper-and hypointense on T2 weighted imaging, lobulated shape and associated with younger age compared with BCA.WT is featured by mild enhancement on the fat-suppressed T1-weighted imaging.A regular tumor with a solid portion showing T2 hypointense signal but marked enhancement will highly favor a diagnosis of BCA in the parotid.tive kinetics and imaging properties of different contrast media used in CT and MR imaging.PAs show marked enhancement on the fat-suppressed contrast-enhanced T1 weighted imaging in our study, which is consistent with the previously reported gradual increased enhancement pattern of PA [9,23] (Table 3).
In our study, the frequency of solid-looking BCAs (33.33%) was lower than that of PAs (54.84%) and WTs (50%).Most of BCAs had a cystic area.The cystic space of BCAs is lined with attenuated thin epithelium and contained some proteinaceous material or hemorrhage [24].Interestingly, we found that more BCAs had an irregular cystic area than PAs and WTs.Notably, this finding has not been previously recorded.

Figure 1 :
Figure 1: A 75-year-old man with basal cell adenoma in both superficial and deep lobes in the right parotid gland.Axial T2 weighted image (a) and axial T1 weighted image (b) show a well-defined, encapsulated, heterogeneous, lobulated tumor with irregular cystic area (arrowheads) and solid nodule (arrows).The solid portion of the tumor shows hypoinentse signal on T2 weighted and T1 weighted images and marked enhancement (arrow) compared with the surrounding parotid gland on axial contrast-enhanced fat-suppressed T1 weighted image (c) but mild enhancement (arrow) on coronal non-fat suppressed T1 weighted image (d) (arrows).

Figure 2 :
Figure 2: A 53-year-old man with basal cell adenoma in the deep lobe of the left parotid gland.Axial T2 weighted image (a) and T1 weighted image (b) shows a well-defined, ovoid solidlooking tumor (arrows).The tumor shows slight hypointense signal on T2 weighted image and T1 weighted image, marked enhancement (arrow) on axial contrast-enhanced fat-suppressed T1 weighted image (c) but mild enhancement (arrow) on coronal non-fat suppressed T1 weighted image (d).

Figure 3 :
Figure 3: A 14-year-old woman with pleomorphic adenoma in the deep lobe of the right parotid gland.T2 weighted image (a) and T1 weighted image (b) show a well-defined, lobulated tumor (arrows).The tumor shows hyperintense signal on T2 weighted image and hypointense signal on T1 weighted image, marked enhancement (arrow) on axial contrast-enhanced fat-suppressed T1 weighted image (c) but mild enhancement (arrow) on coronal non-fat suppressed T1 weighted image (d).

Figure 4 :
Figure 4: A 51-year-old man with pleomorphic adenoma in the superficial lobe of the right parotid gland.T2 weighted image (a) and T1 weighted image (b) show a well-defined, heterogeneous tumor (arrows).The tumor shows hyperintense signal on T2 weighted image and hypointense signal on T1 weighted image, marked enhancement (arrow) on axial contrast-enhanced fat-suppressed T1 weighted image (c) but mild enhancement (arrow) on coronal non-fat suppressed T1 weighted image (d).

Figure 5 :
Figure 5: A 63-year-old man with Warthin tumors in the deep lobe of the left parotid gland.T2 weighted image (a) and T1 weighted image (b) show a well-defined, lobulated, heterogonous tumor.Lesion with irregular cystic area (arrowheads) and solid nodule (arrows).The solid portion of the tumor shows hypoinentse signal on T2 weighted and T1 weighted MR images, and mild enhancement (arrow) on axial contrast-enhanced fat-suppressed T1 weighted image (c) and coronal non-fat suppressed T1 weighted image (d) (arrows).

Figure 6 :
Figure 6: A 74-year-old man with multiple Warthin tumors in the superficial lobe of the right parotid gland and the deep lobe of the left parotid gland.Axial T2 weighted image (a) and axial T1 weighted image (b) show multiple, well-defined, ovoid tumors in bilateral parotid (arrows).The tumors show hypointense signal on T2 weighted and T1 weighted MR images, and mild enhancement (arrow) on axial contrast-enhanced fat-suppressed T1 weighted image (c) and coronal non-fat suppressed T1 weighted image (d) (arrows).

Figure 7 :
Figure 7: Different shape of the cystic areas in the parotid gland tumors.(a) T2 weighted image shows a large ovoid cystic hyperintense cystic area (arrow) in a basal cell adenoma of a 57-year-old man.(b) T2 weighted image shows several ovoid cystic hyperintense cystic areas (arrows) in Warthin tumors of a 52-year-old man.(c) T2 weighted image shows a small round cystic hyperintense cystic area (arrow) in the heterogeneous pleomorphic adenoma of a 39-year-old female with on.(d) T2 weighted image shows a small ovoid cystic hyperintense cystic area (arrow) in a Warthin tumor of an 84-year-old man.

Table 1 :
Characteristics of patients with BCA, PA and WT.Data are expressed as mean ± standard deviation for continuous variables or numbers of patients with percentages in parentheses.† P value by the continuity corrected Chi-square test; ‡ P value by Fisher's exact test; # P value by Mann-Whitney U test.BCA: Basal cell adenoma; PA: Pleomorphic adenoma; WT: Warthin tumor.

Table 2 :
MR Imaging findings of BCAs, PAs and WTs.Data are expressed as mean ± standard deviation for continuous variables or numbers of lesions with percentages in parentheses.