Diagnostic value of gadolinium-enhanced dynamic MR imaging for parotid gland tumors

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ORIGINAL ARTICLE

Diagnostic value of gadolinium-enhanced dynamic

MR imaging for parotid gland tumors

Hazem M. El Shahat, Hadeer S. Fahmy, Ghada K. Gouhar

*

Department of Radiology, Faculty of Medicine, Zagazig University, Egypt Received 10 August 2012; accepted 16 February 2013

Available online 15 March 2013

KEYWORDS Dynamic MR imaging; Parotid gland tumors

Abstract Objective: This study aimed to evaluate the value of gadolinium-enhanced dynamic MR imaging for differentiating benign and malignant parotid gland tumors, and for characterizing the various histological types.

Patients and methods: Non-enhanced T1-weighted (T1-W), fat-suppressed T2-weighted (T2-W), and gadolinium-enhanced fat-suppressed dynamic T1-weighted images were obtained preopera-tively in 27 patients (28 parotid gland tumors), by using a 1.5 or 3 T MR imaging unit (GE, Signa Exite). The tumor margins and the enhancement curve patterns on dynamic MR imaging were ana-lyzed. All patients underwent a parotidectomy with histopathologic analysis.

Results: Pleomorphic adenomas depict a gradual enhancement pattern. Warthin’s tumors depict an early peak of enhancement and a high washout pattern. Malignant tumors depict an early peak of enhancement and a low washout pattern.

Conclusion: Gadolinium-enhanced dynamic MR imaging improved the performance of MR imag-ing in differentiatimag-ing benign from malignant parotid gland tumors and characterizimag-ing the different histological types of benign tumors.

Ó 2013 Production and hosting by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear Medicine.

1. Introduction

It is clinically important to determine whether a salivary gland tu-mor is benign or malignant preoperatively, because this

informa-tion strongly influences the surgical procedure. Local excision or superficial parotidectomy is performed to treat benign tumors, whereas total parotidectomy with or without removal of the fa-cial nerve tissue is performed to treat malignant tumors(1). Pre-operative aspiration cytology is a minimally invasive procedure; however, the results are not always conclusive because insuffi-cient specimens are sometimes obtained owing to a small sample size or the deep location of the tumor(2). Moreover, intraopera-tive frozen section analysis in patients with parotid carcinoma is significantly superior to the aspiration cytology(3). Therefore, preoperative imaging has an important role in surgical planning. The static MR imaging characteristics of malignant salivary gland tumors are reportedly irregular tumor margin, signal

* Corresponding author. Tel.: +20 01010109902.

E-mail addresses:ghadagouhar@hotmail.com,ghadagouhar@yahoo. com(G.K. Gouhar).

Peer review under responsibility of Egyptian Society of Radiology and Nuclear Medicine.

Production and hosting by Elsevier

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology and Nuclear Medicine

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0378-603XÓ 2013 Production and hosting by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear Medicine.

http://dx.doi.org/10.1016/j.ejrnm.2013.02.007

Open access under CC BY-NC-ND license.

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intensity heterogeneity, and tumor infiltration into the sur-rounding tissue(4–6). Freling et al.(7)reported that tumor mar-gins, and signal intensity were not discriminative factors to predict benign or malignant disease. Infiltration into deep struc-tures was observed only in patients with malignant tumors. Thus, the role of static MR imaging in the differentiation of be-nign and malignant salivary gland tumors appears to be contro-versial, except with regard to infiltration into deep structures.

The purpose of our study was to evaluate the diagnostic va-lue of gadolinium-enhanced dynamic MR imaging for differ-entiating benign and malignant parotid gland tumors, and for characterizing the various histological types (pleomorphic adenoma, Warthin’s tumor and malignant tumors).

2. Patients and methods

This study involved 28 parotid gland tumors (Table 1) in 27 patients (17 woman, 10 men; age range 32–71 years). All pa-tients had undergone pathological examination. The distribu-tions of benign and malignant tumors are shown inTable 1. All MR imaging examinations were performed using a 1.5 or 3 T imaging unit (GE, Signa Exite). Non-enhanced T1-weighted (T1-W), fat-suppressed T2-weighted (T2-W), and gadolinium-enhanced fat-suppressed dynamic T1-weighted images were ob-tained for all patients. The section that included the maximum diameter of the tumor was selected for dynamic imaging. Fifteen acquisitions of 11 s scan time each were performed (total acqui-sition time 2.5 min). The region of interest for signal intensity measurement was approximately 3–4 mm in diameter in most cases. Thereafter, time-signal intensity curve (TIC) was ob-tained for all tumors. Three characteristic TICs were observed. TIC parameters include T peak (time of peak enhancement) and WR (washout ratio). In type A, TIC tumor type, the T peak was longer than 120 s. This was considered a gradual enhancement. In type B, TIC tumor type, the T peak was shorter than or equal to 120 s and the WR was greater than or equal to 30%. This was considered as early enhancement and high washout. In type C, TIC tumor type, the T peak was shorter than or equal to 120 s and the WR was less than 30%. A parotid gland tumor with this pattern was considered to have early enhancement and low washout. The TIC type of each parotid gland tumor was deter-mined before surgery in all patients. Finally, all MR imaging examinations together with the tumor specific curves were corre-lated with the histopathologic diagnosis.

3. Results

All tumors with a T peak longer than 120 s were benign, and tumors with a T peak shorter than 120 s were either benign

or malignant. We chose 120 s as the cutoff T peak to maximize accuracy. To distinguish malignant from benign lesions, we chose 30% as the cutoff WR on the basis of the high accuracy measure. (Table 2) shows the distributions of benign and malignant tumors among the three TIC tumor types. Pleomor-phic adenomas depict gradual enhancement pattern, (type A) TIC (Fig. 1). Warthin’s tumors depict an early peak of enhancement and a high washout pattern, (type B) TIC (Fig. 2). Malignant tumors depict an early peak of enhance-ment and low washout pattern, (type C) TIC (Fig. 3). 4. Discussion

The therapeutic strategy for a parotid mass includes identifica-tion of the mass by sonography, CT, MRI, or nuclear medi-cine, and histological diagnosis through biopsy(8).

Preoperative diagnosis of parotid gland tumors plays an important role in surgical planning because surgeons use a more aggressive approach to treat malignant tumors(9).

Among parotid masses, pleomorphic adenoma accounts for about 70% of all lesions and the next most common is War-thin’s tumor. Pleomorphic adenomas have malignant potential. It has been established that nearly 25% of all pleomorphic ade-nomas may eventually become malignant if not treated. There-fore, pleomorphic adenomas must be completely resected. In contrast, malignant change is extremely rare in Warthin’s tumors, so it is clinically important to make a diagnosis of this tumor(10).

The surgery chosen for the treatment of parotid gland tu-mors depends on the location and histologic type of the tumor

(11).

The treatment plan differs slightly depending on whether the tumor is a pleomorphic adenoma or a Warthin’s tumor. Superficial parotidectomy with preservation of the facial nerve or partial superficial parotidectomy is recommended in patients with pleomorphic adenoma, whereas enucleation or superficial parotidectomy with preservation of the facial nerve is adapted for patients with a Warthin’s tumor(12–14).

When the tumor is malignant, total parotidectomy is se-lected and the facial nerve may be sacrificed. Therefore, preop-erative differentiation between benign and malignant tumors is very important(8).

The results of preoperative aspiration cytology are some-times inconclusive or false. Thus, the ability to predict the exis-tence of benign or malignant tumors on the basis of imaging findings would be very useful(15).

Table 1 Histopathologic diagnoses of parotid gland tumors.

Diagnosis No. of lesions Benign (n = 18)

Pleomorphic adenoma 12

Warthin’s tumor 6

Malignant (n = 10)

Mucoepidermoid carcinoma 6 Adenoid cystic carcinoma 3 Carcinoma ex pleomorphic adenoma 1

Table 2 TIC patterns (A, B, C) among histopathologic diagnoses.

Diagnosis TIC patterns

A B C Benign (n = 18) Pleomorphic adenoma (n = 12) 12 Warthin’s tumor (n = 6) 6 Malignant (n = 10) Mucoepidermoid carcinoma (n = 6) 6 Adenoid cystic carcinoma (n = 3) 3 Carcinoma ex pleomorphic adenoma (n = 1) 1

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Fig. 1 Pleomorphic adenoma of the left parotid gland in a 39-year-old woman. (a) Transverse T1-weighted spin-echo MR image shows a well defined hypointense mass in the left parotid gland. (b) Transverse T2-weighted fast spin-echo MR image shows a hyperintense mass. (c) Transverse T1-weighted spin-echo MR image obtained 120 s after contrast material administration shows moderate tumor enhancement. (d) Transverse T1-weighted spin-echo MR image obtained 300 s after contrast material administration shows gradual tumor enhancement. (e) TIC and corresponding transverse T1-weighted spin-echo MR image depict gradual enhancement pattern (type A). The round cursor marks the region of interest selected for signal intensity measurement at dynamic MR imaging.

Fig. 2 Warthin’s tumor of the right parotid gland in a 57-year-old woman. (a) Transverse T1-weighted spin-echo MR image shows a low signal intensity mass in the right parotid gland. (b) Transverse T1-weighted spin-echo MR image obtained 60 s after contrast material administration shows early enhancement. (c) Transverse T1-weighted spin-echo MR image obtained 300 s after contrast material administration shows washout enhancement. (d) TIC and corresponding transverse T1-weighted spin-echo MR image depict an early peak of enhancement and a high washout pattern (type B). The round cursor marks the region of interest selected for signal intensity measurement at dynamic MR imaging.

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The static MR imaging characteristics of malignant salivary gland tumors are irregular tumor margin, signal intensity heterogeneity, tumor infiltration into surrounding tissue, and low signal intensity on T2-weighted images, although there was some overlap(16–18). Thus, the role of static MR imaging in the differentiation of benign and malignant parotid gland tumors appears to be controversial.

The aim of this study was to assess the possibility of diag-nosing parotid masses by imaging alone, using gadolinium-en-hanced dynamic MR imaging.

Takashima et al.(19)reported the results of performing dy-namic MR imaging in the evaluation of head and neck lesions. They examined 43 parotid gland lesions by using dynamic MR imaging and assigned the lesions to five groups according to the type of TIC: type A, curve peaks 0–30 s after contrast material administration; type B, curve peaks at 30–608 s; type C, curve peaks at 60–120 s; type D, gradual upward slope; and type E, flat. These authors classified tumors according to Tpeak only. According to their results, only 4 of 21 pleomor-phic adenomas showed an early enhancement peak at fewer than 60 s after contrast material administration; 8 of 10 War-thin’s tumors showed a peak at fewer than 60 s; and 5 of 11 malignant tumors showed gradual enhancement.

Yabuuchi et al. (15) examined 25 parotid gland lesions using dynamic MR imaging. Their results appear to be consis-tent with those of Takashima et al.(19)in terms of the long Tpeak for pleomorphic adenomas and the short Tpeak for Warthin’s tumors, but different from their results in terms of the Tpeak values for malignant tumors.

Tsushima et al.(20)examined 18 parotid gland tumors by using dynamic MR imaging. According to their results, seven

pleomorphic adenomas and two adenoid cystic carcinomas showed gradual enhancement during the first 260 s after contrast material administration; seven Warthin’s tumors showed rapid enhancement during the first 20 s and then a de-crease in signal intensity. The other malignant tumors showed a rapid increase in signal intensity during the first 20 s and then a gradual decrease or increase in signal intensity.

Takashima et al.(19)concluded that dynamic MR imaging contributes little to the prediction of malignancy but can help narrow the differential diagnosis and is potentially useful in determining tumor vascularity.

Tsushima et al.(20)concluded that dynamic MR imaging could help distinguish pleomorphic adenoma from the War-thin’s tumor but not pleomorphic adenoma from adenoid cys-tic carcinoma or Warthin’s tumor from other malignant tumors. Both Takashima et al. (19)and Tsushima et al.(20)

reports, focused on the Tpeak for parotid gland tumors. Yabuuchi et al.(15)analyzed other TIC parameters as well as the Tpeak and correlated these parameters with histopatho-logic findings. According to their results, Tpeak correlated clo-sely with microvessel count and the WR accurately reflected the cellularity-stromal grade. The microvessel count is consid-ered to represent tumor vascularity, and the Tpeak will be short if the microvessel count is high. The WR depends on the difference in the amount of contrast material within the tu-mor between the intravascular and extravascular phases. A large extracellular space with fibrous stroma retains contrast material for a certain period. Therefore, tumors with a high cellularity-stromal grade will retain less contrast material and have a high WR, whereas those with a low cellularity-stromal grade will have a low WR.

Fig. 3 Mucoepidermoid carcinoma of the right parotid gland in a 56-year-old man. (a) Transverse T1-weighted spin-echo MR image shows a well defined hypointense massin the right parotid gland. (b) Transverse T2-weighted spin-echo MR image shows slightly heterogenous hyperintense mass. (c) Transverse T1-weighted spin-echo MR image obtained 60 s after contrast material administration shows early enhancement. (d) Transverse T1-weighted spin-echo MR image obtained 300 s after contrast material administration shows delayed washout. (e) TIC and corresponding transverse T1-weighted spin-echo MR image depict an early peak of enhancement and a low washout pattern (type c). The round cursor marks the region of interest selected for signal intensity measurement at dynamic MR imaging.

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In our study, we analyzed Tpeak and WR, and according to the results of our study, a Tpeak of 120 s enabled the differentiation of pleomorphic adenomas from malignant tumors. Assessment of the Tpeak alone did not enable differ-entiation of Warthin’s tumors from malignant tumors. The WR for Warthin’s tumours were higher than those for the malignant tumors. Therefore, the combined assessment of Tpeak and WR enabled the differentiation of pleomorphic adenomas, Warthin’s tumors and malignant tumors. TIC types’ classification according to Tpeak and WR had similar results to Yabuuchi et al.(15).

We conclude that the Tpeak and WR derived from TICs at gadolinium-enhanced dynamic MR imaging shows high value in the characterization of parotid gland tumors. A long Tpeak for pleomorphic adenomas, a short Tpeak and high WR for Warthin’s tumors and a short Tpeak and low WR for malig-nant tumors were observed in most instances.

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