MR imaging of salivary glands

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1 Magn Reson Imaging Clin N Am 10 (2002) MR imaging of salivary glands Gaurang V. Shah, MD Department of Radiology, University of Michigan, Room B1G308, 1500 East Medical Center Drive, Ann Arbor, MI 48105, USA Diagnostic imaging of salivary glands has been revolutionized with the advent of cross-sectional imaging modalities like CT and MR imaging. In the era before CT, imaging of the salivary glands was relatively unrewarding and was used uncommonly by ear-nose-throat surgeons [1,2]. Early diagnostic tests like plain films and sialography evaluated dilated parotid ducts and calculus disease within ducts or glands. Full evaluation of salivary glands, especially deep lobes of parotid gland and masses of minor salivary glands, was not possible by these methods, however. Imaging of the parotid glands has developed significantly since that time. CT and MR imaging greatly compliment physical and endoscopic examinations (and previous favorites like sialography) by direct visualization of previously blind areas of the salivary glands and extension of the disease process in surrounding tissue planes [1 5]. The major salivary glands are three paired parotid, submandibular, and sublingual structures. About 600 to 1000 minor salivary glands are scattered throughout the oral cavity, parapharyngeal spaces, nasopharynx, and trachea. Glands are also found at the upper aero digestive tract, along the nasal cavity, paranasal sinuses, and nasopharynx [6,7]. With excellent spatial resolution and superior soft tissue contrast, MR imaging has major advantages over CT. The multiplanar imaging capability of MR imaging allows it to evaluate the extent of disease and outline the contours of tumors. The stated imaging goals of differentiating intraglandular from extraglandular lesions, benign from malignant lesions, and demarcation of facial nerve with relation to the tumor [8] are better served with MR imaging. The tumor muscle interface is better evaluated with MR imaging than with CT. Unlike CT scanning and sialography, the risks of radiation and iodinated contrast are also non-existent with MR imaging. Beam hardening artifacts from dental fillings often degrade CT images. Even though dental fillings might cause susceptibility artifacts with MR imaging, they are generally away from the region of major salivary glands and therefore does not degrade imaging of major salivary glands. For these reasons MR imaging is the preferred modality for evaluation of suspected neoplasm of salivary glands [1,9 24]. Calcification for stones in the salivary duct is more easily detected by CT, hence it is sometimes preferred for imaging of salivary glands over MR imaging [10,25]. Sialography is considered to be the procedure of choice for evaluation of the ductal system [1,26], although it is not performed frequently due to its semi-invasive nature. Attempts to perform sialography with MR imaging [27 33] have been reported for evaluation of ductal stenosis and gland calculi [27,28]. With MR sialography, however, visualization of small branches of the ductal system was considered to be poor [31]. When typical features are present, MR imaging is also considered to be reliable for making the diagnosis of Sjogren s disease or averting biopsy or sialography [34,35]. MR imaging is considered to be better than positron emission tomography (PET) in presurgical evaluation of benign versus malignant parotid masses [36]. Non-removable bridgework degrades imaging in both CT and MR imaging. MR imaging is also not possible in cases of claustrophobia, cardiac pacemakers, ocular foreign bodies, noncompatible aneurysm clips, and surgical ferromagnetic hardware. Embryology The salivary glands arise as buds from the epithelial lining of the mouth. The parotid gland /02/$ - see front matter Ó 2002, Elsevier Science (USA). All rights reserved. PII: S (02)

2 632 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) appears during the fourth week of gestation in the angle between the maxillary process and the mandibular arch; the submandibular gland appears in the sixth week and the sublingual gland appears during the ninth week in the space between the tongue and the mandibular arch. The buds elongate and form a solid structure. Eventually they branch and canalize, forming ducts, which form before the development of acini. Eventually, with the help of autonomic stimuli, a mesh of unique glandular stroma consisting of epithelial cells, myoepithelial cells, adipocytes, lymphatic channels, and lymph nodes forms into parotid glands [37,38]. The uniqueness of the structure of the parotid gland is attributed to the late development of a capsule incorporating these diverse histologic structures and the periparotid lymph nodes [39,40]. The facial nerve is also embedded within the substance of the parotid gland after its emergence from stylomastoid foramen because of proliferation of glandular tissue around its divisions [37,41,42]. This special embryogenesis is believed to contribute towards development of Warthin s tumor and lymphoepithelial cysts [40]. Normal anatomy Parotid gland The salivary glands are named for their locations. The parotid is named for being anterior and inferior to the ears (para-, around; -otid, ear) [43,44]. The submandibular gland is also called submaxillary and is located in upper neck and the floor of the mouth. The sublingual glands are located above the myelohyoid muscle and below the tongue (Fig. 1). The parotid gland is the largest of the three glands, weighing between 14 gm and 28 gm. It is located on side of face, anterior to the mastoid tip and external auditory canal, and it overlaps the masseter muscle anteriorly [8,45 47]. The parotid gland is inferior to the zygomatic arch and posterior and superior to the angle of the mandible. The salivary ducts are organized in a branching system of acini and ducts. The main parotid duct is Stensen s duct (discovered by the Danish anatomist and geologist in 1660), which enters the oral cavity through buccal mucosa opposite upper second molar after coursing over masseter muscle and piercing the buccinator muscle (Fig. 2) [2,7,26]. Fig. 1. (A) Normal anatomy. 1. Parotid salivary gland; 2. Masseter muscle; 3. Stensen s duct; 4. Tongue; 5. Wharton s duct; 6. Sublingual salivary glands; 7. Mandible; 8. Mylohyiod muscle; 9. Anterior belly of digastric muscle; 10. Submandibular salivary gland; 11. Hyoid bone; 12. Posterior belly of digastric muscle. (B) Axial anatomy. A. Superficial lobe of parotid gland; B. Deep lobe of parotid gland; C. Facial nerve; D. Retromandibular vein; E. External carotid artery; F. Intraglandular lymph nodes; G. Masseter muscle; L. Lateral pterygoid muscle; M. Medial pterygoid muscle; N. Temporalis muscle; O. Longus coli muscle; P. Parapharyngeal space; Q. Retropharyngeal space; R. Mastoid process; S. Mandibular ramus. (Illustrations by William Weadock, MD, University of Michigan, Ann Arbor, MI.)

3 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 1 (continued ) The accessory parotid gland is seen in about 20% of population. It usually lies adjacent to the parotid duct and overlying masseter muscle (Fig. 3) [6,48,49]. Rarely, it is a site for development of a tumor [50], accounting for 1% [51] to 7.7% [52] of all parotid gland tumors, which often masquerade clinically as nonsalivary tumors because they are considered to be far too anterior for a parotid mass. This location is important because the buccal branch of the mandibular (V3) division of the trigeminal nerve courses through this region, hence it is susceptible for peritumoral extension [5]. The facial nerve emerges from stylomastoid foramen and gives off smaller posterior auricular, posterior digastric, and stylohyoid nerves. The main trunk travels along the posterior belly of digastric muscle and enters the parotid gland posteriorly after passing through a small amount of fat [22,53]. Within the substance of the gland it passes lateral to the external carotid artery and retromandibular vein, giving off several smaller branches [29,54,55]. Normal facial nerves are not seen on CT; however, they are consistently demonstrated on MR imaging [22,56,57]. The parasympathetic secretary afferents emerge from the inferior salivary nucleus and travel with the glossopharyngeal nerve. They course by way of the Jacobson s plexus in the middle ear to synapse in the otic ganglion. The postsynaptic fibers reach the parotid gland by way of the auriculotemporal nerve. There is no anatomic division of the parotid gland in superficial and deep lobes; no capsule or fascia separates the lobes [58]. Only the plane of facial nerve defines the superficial and deep lobes of the parotid gland [29]. It is suggested that the lobes should be called superficial and deep portions of the parotid gland [44,59]. The deep lobe extends medially inward toward the pharyngeal wall by passing through the stylomandibular tunnel, which is formed between the styloid process and mandibular ramus. The deep lobe then extends in the parapharyngeal space [22]. The superficial portion of the gland is somewhat flattened and quadrilateral in shape, placed between the mandibular ramus in front and the mastoid process and sternocleidomastoid muscle behind. The location of a mass within a superficial or deep lobe of the gland determines the surgical approach. Because the mass of salivary glands is usually treated with surgical excision, the goal of MR imaging is to confirm the location of the mass and to evaluate its relationship with surrounding structures, especially the facial nerve [45,49,58,60,61]. Lesions in the superficial lobe are treated by superficial lobectomy, whereas deeper lesions require total parotidectomy [29,43]. In both the cases, preservation of the facial nerve and its relevant branches is one of the stated goals of surgery in this region, hence the prime objective of imaging [10,62,63]. The course of facial nerve can be approximated by

4 634 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 2. Normal MR anatomy. (A) T1-weighted axial image of parotid gland. (B) T2-weighted axial image of parotid gland. (C) T1-weighted axial image of submandibular gland. (D) T2-weighted axial image of submandibular gland. (E) T1-weighted coronal image of submandibular glands. (F) T2-weighted axial image for sublingual gland (arrow). (G) T1-weighted coronal image showing normal facial nerve (arrow). the retromandibular vein [3,63]. A plane of low signal in expected location on MR imaging is thought to represent the facial nerve [55,64,65]. Visualization of the intraparotid facial nerve is difficult, however, because intraglandular ducts and tributaries of facial veins can have a similar appearance [62,66]. The reliability of imaging in predicting the course of the facial nerve is also affected by possible large masses, which can cause distortion of normal anatomic structures [46,67, 68]. Imaging of intraparotid segments of the facial nerve can be rewarding in cases of isolated

5 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 2 (continued ) peripheral facial nerve palsy with normal special functions like lacrimation, anterior tongue taste, and stapedial reflex [2,3]. Submandibular gland Paired submandibular glands are the second largest salivary glands, about half the size of parotid glands. They are located beneath the floor of the mouth, posterior and inferior to the mylohyoid muscles and superior to digastric muscle [69,70]. Submandibular glands are mixed serous and mucous glands. The lingual nerve and submandibular ganglion are superficial to the gland; the facial nerve lies lateral to it, and the hypoglossal nerve lies medial to it [40]. The lingual artery is medial to the gland and the facial artery is lateral to it. The gland drains into submandibular nodes [71]. Short submandibular ducts, also called Wharton s ducts, run along the floor of the mouth in sublingual space and opens near the lingual frenula. The flow of salivary secretions in this duct is against gravity. The flow also makes sharp angulations in the sagittal and axial planes, hence the

6 636 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 3. Accessory parotid gland. (A, B) Axial T2-weighted and fat-saturated post-gadolinium T1-weighted MR show separate lobule of normal parotid tissue overlying superficial part of right masseter muscle along the course of parotid duct. submandibular gland is more susceptible to stone formation, inflammation, and sialectasia [69]. Sublingual glands The sublingual glands, the smallest paired salivary glands, are located below the mucous membrane of the floor of the mouth, adjacent to mandible, superior to mylohyoid muscle, and lateral to geniohyoid muscle [22,25,72]. About 10 to 12 small-caliber ducts drain the gland. Some drain into the submandibular duct, whereas others empty into the floor of the mouth. Some of these minor ducts might fuse to form a Bartholin s duct, which opens in to submandibular duct [6,26]. Minor salivary glands Small collections of mixed seromucous salivary gland tissues are scattered throughout the oral and nasal cavities and can also be seen in the pharynx, supraglottis, and paranasal sinuses. Tumors arising from these glands have a higher incidence of malignancy than those arising in larger salivary glands [73]. MR imaging technique and appearance Most of the images in this study were acquired with a 1.5 Tesla superconductive magnet with a standard quadrature head coil. Pulse sequences and imaging options are listed in Table 1. Most sequences were obtained by 3 mm slice thickness with 0.5 mm to 2 mm interslice gaps (Table 1). Postcontrast fat-suppressed images enabled evaluation of possible perineural spread of salivary gland malignancy. T1-weighted imaging of parotid glands lends better tissue contrast because of presence of adipose cells within the stroma, yielding high T1 signals. T2-weighted and postcontrast fat-suppressed imaging with T1 weighting is also recommended. Because fat also has high T2 signal on fast spin echo imaging, fat suppression on T2- weighted images helps to bring about tissue specificity [74]. Axial and coronal views are generally obtained. Nonenhanced T1-weighted images combined with nonfat-suppressed fast spin-echo (FSE) T2-weighted images are optimal for delineation of lesions and prediction of the nature of parotid gland pathology [75]. T1-weighted and T2-weighted phase contrast imaging of parotid masses allows greater tissue lesion contrast, but there is no advantage in lesion detectability [76]. The value of giving contrast is not universally accepted [74]. The normal contrast between a normal gland and tumor might reduce because of contrast [5]. Benign tumors like Warthin s and some malignant tumors might not be enhanced [74]; this very characteristic is also considered to be diagnostic by some [56]. Contrast administration helps to distinguish between solid and cystic lesions [40] and it also is

7 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Table 1 Pulse sequences and imaging options Series description Sag T1 Axial flair Pulse sequence Eff. TE Min Full (14) Rep. time (TR) Field-ofview Scan thickness Interscan spacing Acq. matrix (freq.) Acq. matrix (phase) Frequency direction Imaging time Axial T2 A Diffusion B1000 Axial T1 pre/post Coronal T1 post Gd Axial T1 (F-Sat) post Gad SE FSE-IR FSE DW EPI SE SE SE SE Axial T1 post Gd whole head Minimum Min Min Min Min full (14) full (14) full (14) full (14) ,000 10, (18) S/I A/P A/P R/L A/P S/I A/P A/P 1 NEX\1:34 1 NEX/2:20 2 NEX\3:18 1 NEX\1:40 2 NEX\5:18 2 NEX\4:48 2 NEX\3: NEX:\1:27 Contrast No No No No Pre/post Yes Yes Yes helpful in evaluating possible perineural extension of a disease process [18,26]. Contrast administration also helps to evaluate the margins of the mass and its extension into surrounding tissue planes [11,14,22,63]. In inflammatory conditions, however, there is no diagnostic advantage [58]. Postcontrast T1 imaging with suppression of fat is useful in evaluating tumor margins and assessing perineural spread [56]. Newer imaging techniques Magnetization transfer effect is a variable of the type of pulse, the shape and duration of the pulse, and the amplitude of the pulse and offset frequency. A study using a 2 khz off-resonance pulse of 19 millisecond duration and 10 greater waveform than a 90-degree spin-echo pulse did not find any significant correlation between lesion magnetization ratios of head and neck squamous cell carcinoma and degree of mitosis [77]. Another study using 1 khz off-resonance radio frequency pulse with 18 millisecond duration and 110 Hz bandwidth for evaluation of parotid masses had a more positive outcome, finding that lesion-to-muscle magnetizations ratios, when combined with MR imaging, were more accurate for predicting parotid malignancies. This ratio is considered useful in diagnosing recurrent and secondary tumors [78]. A major function of salivary glands, especially the parotid gland, is to produce isotonic, high sodium, low potassium fluid and secrete it within the oral cavity, a process that can be simply called movement of molecules and water or perfusion. Alteration in blood perfusion also occurs within the gland as a response to various external and internal stimuli. The diffusion-weighted MR imaging quantified by apparent diffusion coefficient (ADC) integrates evaluation of both diffusion and perfusion [79]. A study of normal and diseased salivary glands with ADC mapping showed that ADC values increased in sialoadenitis and decreased in abscess. A correlation was also established between decreases in ADC values and severity of gland damage as seen on T1-weighted images [80]. According to a recent study, malignant pathology appeared to have higher ADC values than normal parotid glands. Benign pathology is reported to have statistically significant higher ADC values when compared with normal parotid glands, compatible with reduction in restricted diffusion [81]. 31-phosphorus MR spectroscopy of salivary malignancies showed a large reduction in creatinine phosphate peak and an increase in

8 638 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) phosphomonoesters, phosphodiesters, and organic phosphates [82]. Congenital anomalies Branchial cleft cyst The most common congenital lesion affecting the parotid space is the branchial cleft cyst [2,39, 83,84], which results from incomplete obliteration of the branchial apparatus. The first branchial cyst might be located within the parotid gland (type I) or might be located outside parotid space along the vestigial tract connecting external ear and pharynx (type II) [2] and might present as periparotid mass. Fistulous connection with the external auditory canal might be patent in type II, but not in type I [22]. Type I brachial cleft cysts are relatively rare compared with type II branchial cleft cysts, which might be related to the lower portion of the parotid gland near the mandibular angle and might account for 95% of branchial anomalies [85]. On MR imaging brachial cleft cysts demonstrate low T1 and high T2 signals and appear as single fluid-filled masses. There is generally no thickening or enhancement of the surrounding rim; however, when infected or having a previous history of infection, thickening and enhancement of the surrounding rim can be present (Fig. 4) [2]. The cysts might present as small masses in the parotid region or as waxing and waning intraparotid abscesses that do not respond well to incision, drainage, and antibiotics [2]. Sometimes it is difficult to distinguish a branchial cleft cyst from an abscess or necrotic malignancy solely on the imaging appearance. It also has been suggested that intraparotid branchial cleft cysts without fistulous connections to the external auditory canal (type I) are actually a lymphoepithelial cysts [40], which might develop in response to any chronic inflammatory disease [86]. Cystic hygroma Cystic hygroma occurs more commonly in the posterior triangle of the neck, but it can involve the parotid gland directly or by local extension (Fig. 5) [7,87,88]. Congenital obstruction of lymphatic drainage presumably leads to formation of lymphangiomatous malformations. On MR imaging, high T2 and low T1 signals are observed. Sometimes an increased T1 signal is observed because of the presence of clotted blood. Fluid fluid levels can also be observed [87]. Ranula A mucous retention cyst caused by an obstructed sublingual or minor salivary gland Fig. 4. First Branchial cleft cyst. (A) T2-weighted axial MR image shows a single rounded cystic lesion with high T2 signal within superficial lobe of right parotid gland. (B) Post-gadolinium imaging shows a nonenhancing low T1 signal area.

9 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 5. Cystic hygroma. (A) Axial CT imaging shows a large cystic mass at left parotid gland extending into deep parotid lobe. (B) T1-weighted axial image shows enlargement of left parotid with intermediate T1 signal. (C) T2-weighted axial image shows high T2-signal cystic mass at left parotid gland. (Courtesy of Joseph Gemmete, MD, University of Michigan, Ann Arbor, MI.) appears as translucent blue swelling in the floor of the mouth [89]. These cysts might also occur because of trauma and rupture of acini caused by backpressure from retained secretions. Similar in appearance to the underbelly of a frog, this cyst is known as a ranula (rana means frog in Latin). Hippocrates described this condition and thought it to be secondary to inflammation. When ranulas herniate through mylohyoid muscle into submandibular or low parapharyngeal space, they are known as plunging ranulas and are in fact pseudocysts. Plunging ranulas are usually

10 640 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) secondary to trauma causing obstruction of salivary ducts. Because of continuous secretion of saliva, backpressure builds up, leading to mucus extravasation. Ranulas exhibit homogenous high T2 and low T1 signals [26]. On CT, ranulas have fluid attenuation and the cyst wall is appreciated (Fig. 6), which might or might not enhance depending on the history of infection. Pneumocele Pneumocele results from retention of large amounts of air in the ductal system or gland parenchyma. This retention occurs with increased intrabuccal pressure and it is associated with the playing of musical instruments like the trumpet or blowing glass. The incidence is also high in children due to retrograde insufflation of air [40]. Sometimes pneumocele results from intervention by sharp objects (Fig. 7). Agenesis Agenesis and hypoplasia of parotid glands are rare and are always associated with xerostomia, sialadenitis, and dental caries [15,41,48,90 92]. Aberrant locations of ectopia of salivary glands include the neck, pituitary, cerebellopontine angle, external auditory canal, anterior mandible, and inner posterior mandible [40,91]. Inflammation and infections Sialoadenitis Acute inflammatory disorders of the salivary glands tend to be viral, as in mumps, or bacterial, as in acute suppurative parotitis, which is commonly due to staphylococci or streptococci [93,94]. Pain and swelling are cardinal clinical signs. On MR imaging and CT, the gland might appear to be enlarged and exhibit abnormally high T2 intensity or attenuation and enhance intensely [94]. There is a general thickening of deep and superficial fascia and infiltration of subcutaneous fat [85]. Fascial thickening of deep cervical fascia and infiltration of cervical fat produces a dirty fat appearance (Fig. 8) [5]. Cellulitis of the gland can lead to formation of a focal abscess [2]. Chronic inflammatory conditions include chronic recurrent sialoadenitis, granulomatous diseases like sarcoid, tuberculosis, syphilis, toxoplasmosis, and actinomycosis, Kimura s disease, and sialolithiasis [7,44,95 98]. Chronic inflammation results in shrinkage of the gland [85]. On MR imaging, the gland exhibits low T1 and low T2 signals [38]. Chronic recurrent parotitis of childhood is characterized by recurrent acute exacerbations that result in slowly progressive destruction of the parotid glands [99]. Reactive lymph nodal enlargements can also be associated with infectious conditions; however, differentiating it from lymphoma can be difficult, especially when other findings specific for inflammation are absent. Calcification is another sign of a chronic inflammatory condition [5]. Because MR imaging has a major disadvantage in its inability to image calcifications, CT is the preferred imaging modality when salivary gland infection is suspected clinically [3,100]. Sialolithiasis Fig. 6. Ranula. Axial post-contrast CT image shows a nonenhancing low attenuating mass in front of right submandibular gland. Note its location medial to myelohyoid. Sialolithiasis is second most common inflammatory disease of the salivary glands after mumps. Patients generally present with pain and swelling. About 80% of sialoliths occur in the submandibu-

11 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 7. Oroparotid fistula. (A) Axial CT image shows low attenuating loculated air extending into the parotid duct (not seen) in a patient who formerly had a large neuro epithelial cyst, which was treated by a witch doctor with a sharp instrument through the mouth. (B) T2 axial MR image with signal void at left parotid gland. (Courtesy of Pramod Phadke, MD, Hospital Universiti Kebaangsan Malaysia, Kuala Lumpur, Malaysia.) Fig. 8. Submandibular duct calculus with sialitis. (A) Post-contrast axial CT image shows diffuse enlargement of left submandibular gland with soft tissue stranding at subcutaneous tissue, with thickening of platysma. (B) A focal calcific density (arrow) is seen at the expected location of left submandibular duct suggestive of calculus.

12 642 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) lar gland (Fig. 8) [101], partly due to greater viscosity of saliva and partly due to a wider lumen, tighter orifice, and uphill course of Wharton s duct and dependent position of the submandibular gland [94]. CT and ultrasound have high sensitivity and accuracy for detection of calculi [102,103]. Fast T2-weighted MR imaging with thin sections is proposed for evaluation of ductal architecture [31,104,105], although tiny calculi within the gland and larger duct might not be detected on MR imaging due to signal void associated with a stone [94]. HIV infection Bilateral parotid enlargement in a patient who has AIDS is largely due to development of benign Fig. 9. Lymphoepithelial cysts in AIDS. (A, B) T1-weighted axial image shows multiple low T1 and high T2 signal masses within enlarged parotid glands bilaterally. (C) Post-contrast axial image exhibits lack of enhancement within focal cystic low T1-signal masses.

13 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) lymphoepithelial cysts (Fig. 9), which have similar imaging appearances to cysts associated with Sjogren s syndrome and might be indistinguishable by imaging criteria [ ]. Large glands with cystic enhancement patterns are seen in both conditions. Microscopically, benign lymphoepithelial infiltrate with areas of cystic degeneration are demonstrated within enlarged intraparotid lymph nodes [26]. Cysts associated with HIV infection are also known as acquired immunodeficiencyrelated parotid cysts [108]. Presence of cervical lymphadenopathy, lymphoid hyperplasia, and lack of autoimmune antibodies favors HIV seropositivity [38,107] in patients who have cystic enlargements of both parotid glands. The enlargement of parotid glands in patients who have positive HIV status might also be due to secondary infection [107], rare neoplasia-like adenoid cystic carcinoma, Kaposi s sarcoma, or large-cell lymphoma [109]. Tuberculosis Tuberculous infection of salivary glands is rare [40], but more common in parotid glands (70%) when it does happen than submandibular (27%) or sublingual (3%) glands [44]. More often the infection is secondary to a known primary focus elsewhere in the body, like the lungs or gastrointestinal tract. Tuberculosis likely involves the gland by way of regional lymph nodes. Imaging findings are nonspecific [40] and include formation of a tuberculous abscess (Fig. 10). Nontuberculous mycobacterial infection of salivary glands is a known entity. It is seen mainly in children and it is associated with cervicofacial adenitis [110]. Radiation sialadenitis can be acute or chronic, and it is associated with xerostomia [40,111]. It can occur secondary to partial (acute) or full (chronic) radiation in oropharyngeal or maxillofacial cancer [112,113]. In acute stages, a high T2 signal is seen because of edema in the swollen parotid gland. In chronic stages, the glands appear to be atrophied, smaller, cellular, and fibrotic [40]. On CT the glands appear to have higher attenuation while MR imaging exhibits low T1 and T2 signals. Autoimmune disease Sjogren s syndrome is a systemic autoimmune disorder characterized by xerostomia and keratoconjunctivitis sicca. A connective tissue disease, usually rheumatoid arthritis or systemic lupus erythematosus [114], also should be present as a part of the syndrome. A characteristic pathologic change is periductal lymphocytic infiltration, which can block the intercalated ducts [115]. This diffuse exocrinal disease mainly affects the salivary and lacrimal glands, and it more commonly affects women who are between the ages of 40 and 60 at the onset [26]. Sialography is more sensitive and specific for diagnosis and exhibits characteristic punctuate or globular pooling of contrast. It is an invasive procedure that might exacerbate the inflammation [35]. MR sialography has shown an encouraging correlation with conventional sialography for staging of this disease, showing punctuate, globular, and destructive patterns [61, ]. Compared to a normal population, patients who have Sjogren s syndrome have a 4400% greater risk of having parotid lymphoma [119]. For this reason, any suspicious soft tissue nodule within the affected parotid gland of a patient who has Sjogren s syndrome must be investigated with aspiration or biopsy to rule out the possibility of lymphoma [94]. MR imaging is helpful in detecting such developments [119]. The MR imaging pattern includes enlarged parotid glands with inhomogeneous speckled or nodular patterns giving rise to a salt and pepper appearance on T2-weighted images [35]. This corresponds to intermediate disease. Early disease patterns might reveal enlarged homogenous glands (Fig. 11). Advanced stages exhibit inhomogeneous glands with overall decreases in T2 signals compared with normal subjects [120]. A characteristic inhomogeneous honeycomb pattern is also described on T2-weighted images [119]. The decrease in signal is thought to represent focal accumulation of lymphocytes and fibrous tissue, while the foci of high T2 signals might represent dilated intraglandular ducts [35]. Premature deposition of fat in salivary glands is associated with Sjogren s syndrome. This deposition is more easily monitored with MR imaging (Fig. 12) [121]. Quantitative analysis of MR imaging for signal intensity has been thought to be useful for diagnosis of Sjogren s disorder [122]. MR imaging is thought to have a high positive predictive value for Sjogren s syndrome [123] and is considered to be useful for noninvasive assessment of patients who have xerostomia [120]. Makula et al considered MR imaging to be unnecessary as a routine method in the diagnosis of Sjogren s syndrome; they consider ultrasound

14 644 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 10. Tuberculous abscess. (A) T1-weighted axial MR image shows enlarged right parotid gland with low signal area extending into the deep lobe of parotid gland. (B) T2-weighted axial MR image exhibits central high signal cavity with patchy high signal at rest of the gland. (C) Post-contrast T1 weighted axial MR image shows intense enhancement of enlarged right parotid gland with central nonenhancing low signal cavity. (Courtesy of Pramod Phadke, MD, Hospital Universiti Kebaangsan Malaysia, Kuala Lumpur, Malaysia.) suitable for both diagnosis and follow-up of patients who have Sjogren s syndrome [124]. Neoplasms Neoplasms of salivary glands constitute less than 3% of all tumors in the body and account for less than 0.1% of all cancer deaths [40,94]. Exposure to radiation is associated with an increased risk of malignant salivary gland tumors [44]. Tumors of the parotid glands arise from diverse tissue elements within the substance of the glands. The elements include fat, lymph nodes, glandular tissue, and vascular and neural elements, broadly segregating tumors in to epithelial (arising from glandular and ductal epithelium) and nonepithelial (arising from other tissue elements) varieties. Various studies suggest that the smaller the salivary gland involved, the greater the possibility of a mass arising from it being malignant [44,125].

15 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 11. Sjogren s syndrome with lymphoma. (A) T1 axial MR imaging shows diffuse enlargement of bilateral parotid glands. (B) T2 coronal MR image shows a high signal at enlarged parotid glands. Note the high T2 enlarged lymph nodes at bilateral jugulo-digastric chain. (C) Fluid-attenuated inversion recovery coronal MR imaging shows enlarged high signal lacrimal glands. (Courtesy of Pramod Phadke, MD, Hospital Universiti Kebaangsan Malaysia, Kuala Lumpur, Malaysia.) Benign tumors exhibit smooth, well-defined borders and homogeneous enhancement on CT and MR imaging [1,3 5,21,39,126]. A well-defined intraglandular mass can also be a small malignancy, however [22,62]. Conversely, benign neoplasms with inflammatory reactions in surrounding tissue can mimic infiltrating malignant masses [127]. The tumor margin thus is not an accurate indicator [62] but a good general guide. Benign tumors grow as painless, slow-growing masses. Smaller low-grade parotid malignancies might also exhibit similar imaging features, however [1,3]. Malignant tumors are painful, they grow rapidly, and they generally have poorly defined margins [1,5,12,49,128,129]. Facial nerve paralysis is more often associated with malignant neoplasms (12 14%) than benign ones [42]. Invasion of muscles of mastication is more suggestive of a malignant process [56,130]. It is suggested that patients who fail to regenerate 6 months after facial nerve paralysis should undergo exploratory surgery for possible perineural spread [131]. Neoplasms occurring in superficial lobes of the parotid gland are more likely to be benign,

16 646 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 12. Chronic Sjogren s syndrome. (A) T1 axial MR imaging shows atrophied heterogeneous parotid gland with fatty infiltration. (B) Axial T2 MR imaging shows numerous small cystic areas, more at right parotid gland. (C) Post-contrast axial CT shows atrophic small heterogeneous parotid glands with fatty infiltration, micro-calcifications, and numerous small cysts. whereas malignant tumors are more likely to occur in the deep lobes of the parotid and other salivary glands [49,132]. Masses from deep lobes frequently project medially between styloid process and pterygoid muscle and displace the fat in parapharyngeal spaces, thus having a characteristic dumbbell shape with constriction at the stylomandibular tunnel [132,133]. The most common tumor arising from deep lobes is pleomorphic adenoma, a benign mass [134]. Evaluation of the shape, margin, internal architecture, capsule-like lining of the mass [135], possible infiltration of surrounding tissue planes, and lymph nodal involvement are important parameters for evaluation of a salivary gland mass with MR imaging. High-grade and aggressive malignancies tend to have low to intermediate signals on T2- and T1-weighted imaging, differentiating them from other tumors of the parotid glands [10,62,127,129]. This is because

17 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 13. Pleomorphic adenoma. (A) T1 axial MR imaging exhibits solitary ovoid well-demarcated left parotid gland mass (arrow). (B) T2 axial imaging exhibits well-defined high T2 signal mass. (C) Post-gadolinium T1 axial imaging exhibits intense and patchy enhancement of the mass (arrow), with nonenhancing cystic area. (Courtesy of Joseph Gemmete, MD, University of Michigan, Ann Arbor, MI.) with higher cellularity, overall water content would be low [57]. A majority of parotid tumors are either benign or low-grade neoplasms, however. MR imaging is useful in delineating malignant tumors but it is not considered to be reliable in predicting the histologic nature of a parotid mass [130]. Benign epithelial neoplasms Pleomorphic adenoma Also known as benign mixed tumors, pleomorphic adenoma is one of the commonest benign epithelial tumors of the parotid gland, accounting for 60% to 70% of all salivary neoplasms [26,49,97]. Pleomorphic adenoma usually presents as a slowgrowing, asymptomatic mass in middle age with a mild female preponderance. It can arise from either a superficial or deep lobe, it is usually well circumscribed, and it has a well-developed capsule. Usually a solitary lesion, it might rarely be bilateral and multicentric [16,49]. In these cases dissemination from prior surgery is considered to be a likely reason [21,136]. Rarely, though, it can have irregular and lobulated margins, especially when the tumors are smaller in size [62,137]. The larger

18 648 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 14. Warthin s tumor. (A) T1-weighted axial MR image shows a well-defined intermediate signal mass. An area of cystic change with low signal is seen at anterior medial margin (arrow). (B) T2-weighted axial image shows mass to be predominantly intermediate signal with an area of cystic change anterior-medially. (C) Post-contrast T1-weighted axial MR image shows minimal patchy enhancement of the solid component (arrow). The cystic component does not enhance. masses display a characteristic lobulated contour and are described as a cluster of grapes because of their appearance in the operative field [138]. They are the most common salivary tumors to have calcification or ossification in the tumor matrix [40]. Pleomorphic adenoma can also contain fat on rare occasions and should not be confused with a more discrete lipoma [22]. On MR imaging, pleomorphic adenoma has a homogeneous appearance, a well-defined capsule, and an intermediate to low T1 signal. The T2 signal is generally high, which sometimes might

19 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 15. Hemangioma. (A) T2 axial MR image shows lobulated bunch of grape-like long T2 cystic lesions involving the whole left parotid gland, extending into the masticator spaces. Note the normal looking right parotid gland. (B) T1 axial imaging exhibits low signal mass arising from left parotid gland. Fatty changes are seen at right parotid gland. (C) Postgadolinium T1 axial MR imaging exhibits intense heterogeneous enhancement from the mass. The right parotid gland also exhibits homogeneous enhancement. (D, E) Coronal pre- and post-t1 MR imaging shows large left parotid mass with intense heterogeneous enhancement. be heterogeneous [22] because of myxoid tissue [136]. Small areas of low signal visualized on MR imaging might represent fibrosis or calcification [84,129]. Presence of calcification in a parotid neoplasm favors pleomorphic adenoma; however, this might not be optimally evaluated with MR imaging because of the inherent limitations of MR imaging to demonstrate calcification. Patchy and intense postcontrast enhancement is one of the features that distinguish pleomorphic adenoma from a Warthin s tumor (Fig. 13) [56]. Sometimes pleomorphic adenoma encroaches on adjacent

20 650 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) muscles, especially when arising from a deep lobe; however, it compresses the muscle towards the ramus rather than invading it [56]. Warthin s tumors Fig. 15 (continued ) Also known as adenolymphoma or papillary cystadenoma lymphomatosum, Warthin s tumor has the second highest incidence of benign salivary gland neoplasia and represents about 5% to 10% of all parotid neoplasms. Warthin s tumor is frequently multiple and bilateral and more commonly seen in males in the fourth to seventh decades of life [5,49,139]. Microscopically, it represents a proliferation of salivary ducts incorporated embryonically in parotid gland lymph nodes [140]. The tumor mass is mainly intraglandular, but it might involve periparotid lymph nodes. On MR imaging, Warthin s tumor appears to be a well-circumscribed lobulated mass, mainly in the tail of the parotid gland. It appears to have intermediate signal on T1-weighted and a high signal on T2-weighted images with frequent cystic transformation (Fig. 14). Sometimes it might involve a periparotid lymph node, in which case differential diagnosis includes a necrotic node and second branchial cleft cyst. Warthin s tumor does not show any significant contrast enhancement or might enhance minimally [56,74]. The tumor extent appears different on proton densityweighted images and T2-weighted images; however, this finding is more supportive in nature than diagnostic [56]. Differential diagnosis of multiple uni- or bilateral parotid gland lesions with similar imaging characteristic includes multiple cavitatory metastatic lymph nodes or lymphoepithelial cysts in Fig. 16. Lipoma. (A, B) Axial and coronal T1-weighted MR images show a well-defined hyperintense lesion arising from superficial left parotid gland. (C) T2 fast spin-echo weighted axial MR image shows the lesion to be bright. (D) Fat suppressed T2 axial MR image shows lack of signal at left parotid lipoma. (Courtesy of James Port, MD, St. Joseph Hospital, Baltimore, MD.)

21 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 16 (continued) patients who are HIV-positive [40]. In cases of relatively solid composition, differential diagnosis includes lymphoma, sarcoidosis, and benign adenopathy [141]. Warthin s tumors are hot on Tc- 99m radionuclide scans opposed to pleomorphic adenomas, metastases, abscess, and squamous cell carcinoma. This distinction helps in presurgical planning [140] of such parotid masses. Oncocytoma also tends to be hot, but it is less usual and mostly unilateral. Fig. 17. Mucoepideroid carcinoma. (A) T1-weighted axial MR image shows an irregular low signal mass at left parotid gland. (B) T2-weighted axial MR image shows a patchy increase in the signal of the mass; however, the normal right parotid is hyperintense to the mass. (C) Post-gadolinium T1 coronal MR imaging shows a patchy heterogeneous enhancement of the mass (arrow); however, the normal right parotid is more intense than the mass.

22 652 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 17 (continued) Hemangiomas represent 1% to 5% of all salivary gland tumors. These are the most common parotid gland tumors of infancy, and they occur predominantly in girls [22,142]. Swelling that is compressible and soft is the commonest presentation. This swelling regresses spontaneously in about half of patients, especially during second and third year of life [49,143]. Hemangiomas might also enlarge rapidly and alarmingly, possibly due to bleeding within. A cutaneous angioma might also be found overlying the parotid region [144] as an associated finding. Hemangiomas can be well circumscribed or can be infiltrative and might involve periparotid musculature. Submandibular gland involvement is rare, but it is also difficult to distinguish from soft tissue extension of a main mass, which is also common. On MR imaging, hemangiomas exhibit intermediate T1 and high T2 signals. Presence of flowvoids denotes enlarged blood vessels [144]. Large calcifications, likely phleboliths, when present, help to differentiate hemangiomas from lymphangiomas (Fig. 15) [129,144]. Benign nonepithelial neoplasms Hemangioma Lipomas Lipomas represent about 1% of all parotid tumors and occur in all age groups. They can be discrete or (less likely) infiltrative. In more than 90% of cases, the lesion is well circumscribed and homogenous and displays a characteristic high T1 and low T2 signal on MR imaging (Fig. 16) [62,145]. Lipomas can be excised surgically but Fig. 18. Adeno cystic carcinoma. (A) T1-weighted axial MR image shows lobulated primarily low signal mass in the right parotid gland extending into the deep lobe. (B) Fat suppressed T2 axial MR image shows the lesion to be heterogeneously hyperintense with a few markedly bright areas. (C) Post-gadolinium T1 axial MR image shows intense enhancement of the lesion.

23 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Mucoepidermoid carcinoma is the most common salivary gland malignancy, accounting for nearly one third of malignant tumors [49], but less than 10% of tumors overall [40]. Nearly half of these tumors occur in parotid glands and half occur in minor salivary glands of palate and mucosa [44,127,150]. They occur predominantly in the fifth decade of life [151], but they are the most common salivary malignant tumors in children [26,44,127]. They can be low-, intermediate-, or high-grade malignancies and they have variable clinical courses. The well-differentiated variety of mucoepidermoid carcinoma is generally better circumscribed and displays a high T2 signal. The poorly differentiated types are more aggressive and infiltrative. On MR imaging, the well-differentiated type can have relatively well-defined margins, a high T2 signal, and (sometimes) cystic areas within it (Fig. 17) [40]. The poorly differentiated variety tends to be infiltrative and aggressive, has indistinct and irregular margins, and a low T2 signal [57]. have a tendency to recur [49]. A lipoma is more discrete and should not be confused with a pleomorphic adenoma, which can contain fat on rare occasions [22]. Infiltrative lipoma and diffuse lipomatosis syndrome are indistinguishable from each other [41,44]. Schwannomas or neurofibromas are neurogenic tumors of the salivary gland, usually the parotid gland. Multicentricity favors neurofibroma [129,146]. Scattered low-signal foci within the mass likely represent calcification. Solitary fibrous tumor of the parotid gland is a rare benign fibroma [147]. Polycystic disease of the parotid gland is a rare disorder and shows marked enlargement of the parotid glands with an increased T2 signal [148]. Primitive neuroectodermal tumor of parotid gland has also been reported [149]. Malignant tumors Fig. 18 (continued) Mucoepidermoid and adenocystic carcinoma are the most common low-grade epithelial malignancies. Malignant epithelial tumors are classified into low, intermediate, or high grade [49]. Mucoepidermoid carcinoma Adenoid cystic carcinoma Adenoid cystic carcinoma is the most common malignant tumor of the submandibular and minor salivary glands, accounting for 4% to 8% of total salivary gland tumors [22,26,40,151]. It occurs predominantly between fourth and sixth decade of life, and it is usually a slow-growing tumor, though it often has a poor clinical outcome. On MR imaging, parotid gland tumors appear relatively well defined and have high T2 signals due to higher water content (Fig. 18). Tumors arising from minor salivary glands tend to have irregular margins. The perineural spread can be assessed by the thickening of the nerve or postcontrast enhancement, which are seen much more distinctly on fat-saturated T1 imaging following contrast administration [40,56]. Perineural invasion and recurrence are frequent; sometimes perineural invasion occurs after surgical removal of the gland (Fig. 19) [49,151]. Ex-pleomorphic adenoma is malignant transformation of pleomorphic adenoma and occurs in 2% to 5% of all cases of these mixed tumors. Adenocarcinoma, squamous cell carcinoma, salivary duct carcinoma, acinic cell adenocarcinoma, epithelial myoepithelial carcinoma, and undifferentiated carcinoma are relatively rare primary malignant tumors of the salivary gland; all have poor outcomes [95,96,127,132,152]. Rhabdomyosarcoma, fibrosarcoma, angiosarcoma, synovial sarcoma, fibrohistiocytoma [129], and malignant myoepithelioma [153] are rare sarcomatous primary malignancies of the major salivary glands and appear similar to lymphoma on MR imaging.

24 Fig. 19. Adeno cystic carcinoma with perineural spread. (A) T1-weighted axial image shows ill-defined mass along the anterior left parotid gland, overlying left masseter muscle (arrow). (B) T2-weighted image shows the mass has marginally high T2 signal. (C) Post-contrast fat-saturated T1 image shows intense contrast enhancement along the buccal branch of left mandibular nerve (V3), compatible with perineural spread.

25 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Primary lymphoma Primary lymphoma of salivary gland can be considered only if there is histologic proof of involvement of the salivary parenchyma without involvement of the intraparotid or extraparotid lymph nodes. This extremely rare condition occurs in the fifth to sixth decade of life and has female predominance [40]. Mucosal-associated lymphoid tissue (MALT), also called MALToma or MALT lymphoma, is a monocytoid, non-hodgkin s B-cell lymphoma (Fig. 20) arising in extranodal sites like the salivary gland, thyroid, and stomach, which lack native lymphoid tissue. MALT lymphomas occur in close association with chronic inflammation like myoepithelial sialadenitis or autoimmune processes like Sjogren s disease [154]. Secondary lymphoma Secondary involvement of the parotid glands caused by systemic lymphoma is more common. The incidence of lymphoma is 40 higher in patients who have Sjogren s disease than in the general population [146], and the prognosis is poor [155]. Large-cell lymphoma is more likely to affect the parotid gland than non-hodgkin s Fig. 20. Mucosal-associated lymphoid tissue lymphoma. (A) Axial T1 MR image shows heterogeneous low signal mass at posterior part of the left parotid gland. (B) Axial fat suppressed T2 MR image shows a few hyperintense areas within the high signal mass. Note the normal looking anterior part of the left parotid. (C) Post-contrast axial T1 MR image shows patchy enhancement of solid left posterior parotid mass with a few nonenhancing areas.

26 656 G.V. Shah / Magn Reson Imaging Clin N Am 10 (2002) Fig. 21. Large-cell lymphoma. (A) Axial post-contrast CT shows large lobulated patchily enhancing lymph nodes at both parotid glands, larger on the right. (B) Axial post-contrast CT shows numerous lobulated solid lymph nodes at the level of submandibular gland, more on the right. and Hodgkin s lymphoma [44]. On MR imaging, the lymph nodes exhibit homogenous intermediate signal intensity on T1-weighted images and mildly increased or decreased signals on T2-weighted images [5,40]. Discrete intraglandular lymph nodal enlargement is common (Fig. 21). Diffuse infiltration of glandular tissue is rare. Presence of extraglandular lymph nodal enlargements favors a systemic etiology. Intraglandular lymph nodal enlargements are also seen in viral or bacterial lymphadenitis, granulomatous diseases like sarcoidosis, toxo- Fig. 22. Metastatic parotid lymph node (squamous cell carcinoma maxilla). (A) T1-weighted axial MR imaging shows low T1 signal enlarged intraparotid lymph node at right parotid gland. (B) Fat suppressed post-contrast T1 coronal imaging shows patchy enhancement of numerous right parotid lymph nodes, as well as large lymph node at right jugulodigastric chain.