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1 David M. Yousem, MD Major Salivary Imaging Michael A. Kraut, MD, PhD Ara A. Chalian, MD The algorithm for imaging the salivary depends on the clinical scenario with which the patient presents to the clinician. Because of the importance of identifying Index terms: small calculi in the gland or salivary as the cause of the symptom complex, Salivary glands, calculi, 264.818 nonenhanced computed tomography is often the best initial study for the evaluation Salivary glands, CT, 264.12111, of the painful gland. If an infiltrative neoplasm is highly suspected, nonenhanced and 264.12112 Salivary glands, diseases, 264.247 enhanced magnetic resonance (MR) imaging may be superior in demonstrating Salivary glands, MR, 264.12141, perineural, meningeal, and skull base invasion. is reserved for the 264.12143 evaluation of chronic sialadenitides unrelated to . Thin-section MR Salivary glands, neoplasms, 264.363, techniques for MR sialography may soon replace conventional sialography. 264.37

Radiology 2000; 216:19–29

Abbreviations: HIV ϭ human immunodeficiency virus While neoplasms of the major salivary glands constitute less than 3% of all tumors in the SE ϭ spin echo body, many people have an illness related to the salivary glands at some time in their lives. The process may be self-limited, such as with viral or , but in others it may 1 From the Department of Radiology, be a relapsing and remitting illness, such as chronic secondary to sialolithiasis. Johns Hopkins Hospital, 600 N Wolfe Still others may be evaluated for what is thought to be a mass but is actually a St, Houck B-112, Baltimore, MD 21287 mass peripheral to the glands, such as a lymph node. Very rarely, a nonnodal extraglandu- (D.M.Y., M.A.K.), and the Department lar lesion such as a schwannoma, masseteric hypertrophy, or other pseudomass may be mistaken of Otorhinolaryngology: Head and for a glandular process, even by experienced otorhinolaryngologists (1). The purpose of this Surgery, University of Pennsylva- nia Medical Center, Philadelphia review is to illustrate the role of imaging in evaluating diseases of the major salivary glands. (A.A.C.). Received January 22, 1999; The range of studies needed to assess salivary gland lesions spans a wide gamut. Many of revision requested March 30; final the disease processes described above may not require imaging of any kind. Still others may revision received August 6; accepted be readily evaluated with palpation and direct visualization either endoscopically or August 18. Address correspondence to D.M.Y. (e-mail: [email protected]). transorally. At the other end of the spectrum are infiltrative deep lobe parotid masses such ௠ RSNA, 2000 as adenoid cystic carcinomas, which may require computed tomography (CT), magnetic resonance (MR) imaging, and/or conventional angiography as part of a preoperative evaluation for perineural, vascular, or skull base infiltration. Ultrasonography (US), underutilized in most North American sites, may supplant the role of CT and MR imaging for superficial salivary gland lesions when experienced sonographers use the technique. Patients with major salivary gland lesions may present to the otorhinolaryngologist or oral and maxillofacial surgeon with a suspected mass, with a suspected obstruction or , or with diffuse glandular enlargement (2). Although there are overlapping entities in this simple stratification, the imaging studies ordered may change with each presentation. For the purposes of this review, major salivary gland imaging will be divided into neoplastic lesions, obstructive or inflammatory lesions, and systemic diseases.

NEOPLASTIC LESIONS

The usual clinical manifestation of a salivary gland neoplasm is that of an enlarging mass. The first critical step in evaluating a mass is to determine whether or not it is painful. While painful masses may be produced by obstructive or inflammatory disease, the classic painless mass in the salivary glands is usually due to a neoplasm, cyst, or lymph node. A dull, gnawing pain may be produced by some neoplasms in the glands. Other signs that a parotid neoplasm is malignant are infiltration of the overlying skin, regional adenopathy, or facial palsy. Regional lymph node spread is relatively infrequent with salivary gland primary malignancies. There are some general rules that apply to salivary gland neoplasms. The smaller the salivary gland, the higher the rate of malignancy. Thus, the rate of malignancy increases from 20%–25% in the to 40%–50% in the and to 50%–81% in the sublingual glands and minor salivary glands (3–6). Nearly 80% of benign parotid neoplasms are pleomorphic adenomas (3,4). Pleomorphic adenomas, also known

19 Figure 1. Bilateral Warthin tumors. Bilateral parotid masses (arrows) are seen on this trans- verse, contrast material–enhanced, fat-satu- rated T1-weighted spin-echo (SE) (750/30 [rep- etition time msec/echo time msec]) MR image. The multiplicity and location at the tail of the parotid gland (near the lower ) are a. c. typical features of this tumor. Figure 3. Pleomorphic adenomas. (a) Trans- verse T1-weighted SE (600/11) MR image shows the mass (P) to be well highlighted against the normal hyperintensity of the parotid gland. The margination is not particularly sharp, yet the diagnosis was . (b) The mass (P) is hyperintense on this trans- verse, long repetition time (4,000 msec), T2- weighted fast SE MR image. (c) The mass (P ) enhances on this contrast-enhanced, T1- weighted SE (600/30) MR image, though it has a central nonenhancing component.

If there is very strong suspicion that a lesion is neoplastic, there are some com- b. Figure 2. Submandibular pleomorphic ad- pelling reasons why MR imaging may be enoma. Transverse, contrast-enhanced CT scan preferred over other modalities. Virtually shows that the pleomorphic adenoma (A) arises in the right submandibular gland. The attenua- all parotid lesions are well visualized on tion characteristics leave little indication as to the other salivary glands do not. This T1-weighted MR images because of the whether the lesion is benign or malignant. accounts for the potential for malignant hyperintense (fatty) background of the adenopathy involving the parotid glands. gland (Fig 3) (8). The T1-weighted image This is usually seen in the setting of a gives an excellent assessment of the mar- as benign mixed tumors, occur most com- dermatologic malignancy (basal cell carci- gin of the tumor, its deep extent, and its monly in middle-aged women. Monomor- , , and pattern of infiltration. This sequence, phic adenomas and myoepitheliomas are melanoma), but occasionally an upper aero- coupled with fat-saturated, contrast mate- the other common benign tumors and digestive system squamous cell carcinoma rial–enhanced T1-weighted imaging, used may arise in both parotid and submandibu- may result in malignant parotid adenopa- primarily to address perineural spread lar glands. and Warthin tu- thy. The lymph nodes must be deter- (9,10), bone invasion, or meningeal infil- mors are rare outside the parotid region. mined to be intraparotid or extraparotid tration, is the best means for ‘‘mapping’’ Multiple parotid masses are usually due at imaging. By the same token, lym- the tumor. If there is a superimposed to lymphadenopathy or Warthin tumors, phoma may occur primarily in the pa- diffuse inflammatory process, a focal mass the latter appearing almost exclusively in rotid gland as an infiltrative process or could possibly be obscured with this se- the parotid gland, usually in the tail of adenopathy, or as a manifestation of sys- quence. On fat-saturated images, both the gland in older men (Fig 1). The most temic disease. the bone marrow and cortex of the man- common malignancy of the parotid gland Some would advocate the use of MR dible, , and skull base will be is (2,3). In imaging as the first (and only) technique hypointense. Enhancing (hyperintense) the submandibular gland, pleomorphic to evaluate a neoplasm of the major sali- tissue extending into this hypointense adenomas remain the most common be- vary glands. Implicit in such a decision is background is indicative of bone inva- nign tumor (Fig 2), but adenoid cystic that the clinicians are highly confident sion. At the skull base, where the abun- carcinoma is the most common malig- that the process in the gland is neoplastic dant fat and bony foramina will also have nant histologic diagnosis (5). The same and not obstructive or inflammatory. If suppressed signal (low signal intensity), diagnoses prevail in the sublingual and there is even a slight chance that the mass the fat-saturated, contrast-enhanced im- minor salivary glands (7), where malig- may in some way be related to sialolithia- age will show spread of hyperintense nancies outnumber benign tumors. sis, CT should be recommended first, enhancing tumors up the stylomastoid Lymph nodes may manifest as intrapa- since MR imaging is not as reliable in foramen (cranial nerve VII) (Fig 4), fora- rotid masses. Since the parotid gland en- detecting small calculi, and ‘‘pseudo- men ovale (cranial nerve V-3), or foramen capsulates late in the 2nd trimester, it masses’’ may accompany sialolithiasis (see rotundum (cranial nerve V-2). Therefore, incorporates lymphatic tissue, whereas Obstructive or Inflammatory Lesions). if a facial or palsy accom-

20 • Radiology • July 2000 Yousem et al long repetition time images (Fig 8). Some malignancies, however, exhibit elevated signal intensity on T2-weighted images. Most commonly, this is seen in low-grade mucoepidermoid carcinomas (14), in some adenoid cystic carcinomas (15), and rarely in . Among be- nign masses that are not hyperintense on long repetition time images, Warthin tu- mor, the second most common benign mass in the adult parotid gland, is often of intermediate, low, or mixed signal in- tensity on T2-weighted images (8). The chronic sialadenitides, such as Sjo¨gren Figure 5. Seeding of pleomorphic adenoma. disease, Mikulicz disease (also known as Parotid (arrow) and deep lobe or parapharyn- geal (arrowheads) masses are present on the left Sjo¨gren type 1 or sicca syndrome without side on this transverse T1-weighted SE (500/11) a connective tissue disorder), and radia- MR image. The patient underwent prior at- a. tion sialadenitis, may also appear hypoin- tempted resection of a deep lobe pleomorphic tense on T2-weighted images (14). In adenoma, but the capsule of the tumor was most series, these exceptions account for violated. Months later she presented with this the 25% error rate that occurs if one relies picture of tumor infiltrating the operative bed and the surrounding tissue. solely on signal intensity on T2-weighted images to predict histologic diagnosis. The CT attenuation of masses, other than for differentiating benign cysts from with regard to geographic properties such solid masses, and lipomas from other as margins, shapes, and borders (Fig 6) neoplasms (Fig 9), does not help in pre- (12,13), T2-weighted MR imaging has dicting histologic diagnosis since most been shown to be a reasonably reliable malignant and nonmalignant solid (73%) predictor of whether a salivary masses have similar CT attenuation (Fig gland tumor is benign (Fig 7) or malig- 10). Although high-grade malignancies nant (14,15). The conventional wisdom tend to have irregular infiltration into the is that a hyperintense mass on T2- glandular parenchyma (13,16), which can weighted images is benign and a mass of be detected with both MR imaging and b. low to intermediate signal intensity is CT, there are enough exceptions to this Figure 4. Perineural infiltration of cranial malignant. Others have implied that sig- rule that CT has only fair accuracy (60%– nerve VII by . (a) Trans- nal intensity on T2-weighted images is of 70%) in predicting the histologic diagno- verse T1-weighted SE (600/11, two signals ac- little help (4,13). In general, however, the sis of a lesion (17). Because CT appear- quired) MR image shows that the right parotid mass (m) enters the notch of the stylomastoid most common benign tumor of the sali- ance is not a good predictor of histologic foramen (arrow). (b) Coronal, gadolinium- vary glands, the pleomorphic adenoma, diagnosis and since CT is less accurate enhanced T1-weighted SE (600/17, one signal has very high signal intensity on T2- than MR imaging for determining the acquired) MR image shows vertical extension weighted images (Fig 7) (13). Benign cysts extent of disease (16), there is little reason of the enhancing tumor (arrows) through the (mucous retention cyst, lymphoepithe- to advocate CT over MR imaging in the stylomastoid foramen (line is at the plane of lial cyst, first , , setting of a suspected salivary gland mass. transverse image in a). , and pseudocysts) may also be However, neither study can be relied upon hyperintense on T2-weighted images, wholly to predict histologic diagnosis; and, depending on the presence of hem- hence, fine-needle aspiration or biopsy is panies a mass, MR imaging is usually the orrhage, , or hyperproteinaceous usually required to establish the diagno- study of choice. If meningeal symptoms fluid, the T1-weighted image may show sis in the major salivary glands. coexist, MR imaging may also be pre- intermediate (solid-appearing) intensity. Nuclear scintigraphy may help diag- ferred since the leptomeninges are better For this reason, administration of con- nose Warthin tumors (cystadenoma lym- assessed with MR than with CT (11). trast material is helpful because cysts phomatosum) and oncocytomas. These On nonenhanced and enhanced T1- usually enhance on their periphery, tumors are unique in that they show weighted series, no histologic discrimina- whereas pleomorphic adenomas enhance increased radiotracer uptake at techne- tion is possible since almost all masses are solidly (Figs 3c, 7b). The value of contrast tium pertechnetate imaging. Since nei- lower in intensity than the parent gland enhancement applies also to CT because ther of these lesions has substantial malig- and almost all salivary gland neoplasms the attenuation of the cyst may not be nant potential, a course of observation enhance. Deep infiltration into the para- that of pure fluid, particularly when trau- may be advocated in the elderly patient pharyngeal space, muscles, and bone, well matized, infected, or hyperproteinaceous. with surgical contraindications. This is in seen on T1-weighted images, will strongly Most high-grade mucoepidermoid car- contrast to the treatment of pleomorphic suggest malignancy (4) or, less frequently, cinomas, undifferentiated carcinomas, ad- adenomas. Since pleomorphic adenomas rupture of the capsule of a pleomorphic enocarcinomas, and squamous cell carci- have the potential for malignant degen- adenoma (Fig 5). While benign and malig- nomas of the major salivary glands have eration and/or coexistent adenocarci- nant masses exhibit considerable overlap low to intermediate signal intensity on noma, they are treated more aggressively

Volume 216 • Number 1 Major Salivary Gland Imaging • 21 Figure 6. Right submandibular gland adeno- carcinoma. Transverse CT scan shows an exophytic, well-defined mass (M) in the right a. b. submandibular region that proved to be an adeno- Figure 7. Pleomorphic adenoma. (a) Transverse T2-weighted SE (3,000/80, one signal acquired) carcinoma. First and foremost, one should at- MR image shows that the lesion ( ) is hyperintense. This may raise the question of a cyst versus a tempt to determine whether this lesion is a * pleomorphic adenoma. (b) With administration of a gadolinium-containing contrast agent and submandibular lymph node metastasis or a fat saturation, the mass ( ) is seen to enhance avidly on this coronal T1-weighted SE (600/17, one primary lesion from the submandibular gland * signal acquired) MR image, compatible with a solid mass. (as in Fig 2). The anterior , which usually lies between submandibular and extra- glandular masses (1), was not conspicuous in this case. The gland and mass were resected together, and the origin from the submandibu- lar gland was uncovered. Although this lesion was well defined, it was malignant (compare with Fig 2). with surgical extirpation (18). Positron emission tomography (PET) has been studied to see if it can reliably predict histologic diagnosis (19). At an accuracy rate of 69%, PET compared unfavorably with accuracy rates reported for MR imag- ing (14,15,19). Therefore, the role of scin- tigraphy is usually limited to confirming the clinical diagnosis of Warthin tumors in those patients with multiple parotid masses. US is a useful technique to assess super- ficial parotid, submandibular, and sublin- a. b. gual masses (20,21). US is not as readily used in North America, and the expertise Figure 8. Mucoepidermoid carcinoma of the parotid gland. (a) Transverse T2-weighted SE in interpreting sonograms of the head (3,000/90) MR image shows an intermediate-signal-intensity mass (arrow) slightly lower in intensity than that of the native parotid tissue. (b) The ill-defined nature of the mass (arrow) was and neck is not as widespread in the exemplified by the fuzzy margins on this transverse, contrast-enhanced, fat-saturated, T1- United States as it is in Europe and Japan. weighted SE (600/30) MR image. The diagnosis was high-grade mucoepidermoid carcinoma. In appropriate hands, however, US can help analyze superficial salivary gland lesions with the same precision as CT and MR imaging. Gritzmann (22) demonstrated nign (22). US differentiated extraglandu- implies a pleomorphic adenoma (24). The in a blinded retrospective review that 287 lar from intraglandular lesions with an echotexture of is finer than (95%) of 302 space-occupying lesions of accuracy of 98% (all mistakes were peripa- that in benign adenopathy (25). the major salivary glands (285 in the rotid lymph nodes). Other reports have The limitations of US (even in the best parotid, 13 in the submandibular, and confirmed that US also does an excellent of hands) include its inability to evaluate four in the sublingual glands) could be job in enabling distinction of glandular deep parotid masses, lesions obscured by completely delineated at US. All 302 neo- from extraglandular masses (23). This dif- the mandible, parapharyngeal extension, plasms were hypoechoic to normal glan- ferentiation is helpful to the otorhinolar- retropharyngeal and deep neck adenopa- dular tissue. US enabled correct assessment yngologist who may not be able to discern thy, and the intracranial or skull base of whether a lesion was benign or malig- the planes as well by means of palpation. extent of a mass (22). US shows a lack of nant in 272 cases (90%) on the basis of Malignant salivary tumors show a higher specificity for cystic lesions, and the rela- definition of the margins of the tumor, grade of vascularity at color Doppler US tionship of a tumor to the is but 28% of malignant lesions (16 of 58 than do benign tumors (24). Peripheral hard for surgeons to appreciate on US lesions) were misinterpreted as being be- vascularity with a hypovascular center images.

22 • Radiology • July 2000 Yousem et al a.

Figure 10. Mucoepidermoid carcinoma of the Figure 11. Markers for the seventh cranial parotid gland. Transverse CT scan shows an nerve. Transverse T1-weighted SE (500/11) MR ill-defined mass (C) that has less attenuation image shows that the seventh cranial nerve than that of enhancing parotid tissue in the emerges from the stylomastoid foramen to right parotid gland. The attenuation of this course through the fat (straight arrow) immedi- mass is the same as that of the pleomorphic ately below this exit. In its course through the adenoma in Figure 2 and less than that of the parotid gland (p), it runs lateral to the retroman- carcinoma in Figure 6. dibular vein (curved arrow). This is the best sequence for defining anatomic landmarks.

the mass. Though some parotid malignan- sion of the nerve at the stylomastoid cies may manifest with facial nerve im- foramen (or above) prods the surgeon to pairment (24%) (2), a new postoperative plan for transmastoid identification of facial paralysis is the bane of the surgeon the facial nerve to control disease and and the patient. prevent tumor spillage. The superficial Even with thin-section MR imaging, thereby becomes skull base b. there is controversy as to the reliable surgery with its attendant risks (to the Figure 9. Lipomas. (a) Although the attenua- identification of the facial nerve below other cranial , venous sinuses, ca- tion of this patient’s parotid glands is low due the skull base (26–29). Its course is sur- rotid , and to fatty infiltration on this transverse CT scan, mised by its egress from the stylomastoid function) and morbidity. If the nerve at a palpable (see marker superficially) lipoma (L) in the left parotid gland was appreciated. foramen; its passage anterior to the poste- the skull base is invaded, the cartilagi- (b) This lipoma (arrow), hyperintense on this rior belly of the , lateral nous auditory canal may have to be ad- transverse T1-weighted SE (600/11) MR image, to the plane of the stylomandibular tun- dressed and possibly resected. A radical was extraglandular but still contained by the nel, and around the retromandibular vein; mastoidectomy is contemplated and even deep cervical fascia surrounding the gland. and its branching pattern to the muscles the ascending ramus of the mandible of facial expression (30–32) (Fig 11). The may be removed (6). MR imaging does line connecting the lateral surface of the well in demonstrating the perineural, vas- To the surgeon, it is the facial nerve posterior belly of the digastric muscle and cular, and dural invasion that may be that is the critical structure when operat- the lateral surface of the mandibular as- present with parotid malignancies (34). ing on the parotid gland. By contrast, cending ramus has also been used to Adenoid cystic carcinoma has a very submandibular and sublingual glandular separate superficial (lateral to the facial high rate of perineural spread (50%–60%) tumors are removed with relative impu- nerve) and deep (medial to the facial (35). It is the most common malignancy nity. While submandibular and sublin- nerve) parotid masses (33). The differen- to affect the minor salivary glands and gual gland resections can injure the lin- tiation of deep or superficial parotid the , and it is one of the gual nerve or hypoglossal nerve and masses is critical from the standpoint of three most common tumors of the pa- possibly the marginal branch of the facial the extent of dissection needed to sepa- rotid and submandibular glands. Visual- nerve, these deficits are easily compen- rate the nerve from the tumor or to gain ization of the cranial nerves and tumoral sated for by the patient. However, the access to the tumor, the attendant risk to infiltration around these nerves to and consequences of facial nerve injury are so the facial nerve, and, in the case of tu- through the skull base is probably best substantial functionally and cosmetically mors extending into the parapharyngeal evaluated by using nonenhanced and that much effort is directed toward teas- space, the need for a cervical approach gadolinium-enhanced, fat-saturated, T1- ing out the trunk and peripheral branches with or without mandibulotomy (6). weighted MR sequences (9,10,34). of the facial nerve before even addressing Demonstration or suspicion of direct inva- Multiple painless masses in the parotid

Volume 216 • Number 1 Major Salivary Gland Imaging • 23 a. b.

Figure 12. CT-guided aspiration of deep lobe parotid mass. Via a transbuccal approach, the needle passed between the ascending ramus of the mandible and the maxilla, with its tip (arrow) at the edge of the deep lobe parotid mass (P). Several 2-cm thrusts into the mass under syringe suction and transverse CT guid- ance yielded cells compatible with mucoepider- moid carcinoma. The well-defined margins be- lied the malignant nature of the mass.

gland invoke a differential diagnosis of Warthin tumors (Fig 1) (36), multiple pleomorphic adenomas (18), oncocyto- mas, lymph nodes, lymphoma, acinic cell c. d. carcinoma, metastases (37), human im- munodeficiency virus (HIV)–related cysts Figure 13. (a–d) Transverse CT scans of ductal and glandular calcifications. (a) There is a large and nodules (38), and Sjo¨gren syndrome solitary sialolith (arrow) in the right . (b) These glandular calcifications (arrows) could easily be mistaken for vessels on this contrast-enhanced CT scan. (c) Are these (39,40). Lymphoma, associated with Sjo¨- vessels or calcifications (arrows) along this ill-defined monomorphic adenoma of the submandibu- gren syndrome or not, may infiltrate the lar gland? (d) Image obtained with bone window settings is equivocal due to the small size of the entire parotid gland or present as mul- opacities (arrows), but the nonenhanced scans showed that the posterolateral one was a tiple lymph nodes in the gland. Cystic calcification and the anteromedial structure was a vessel, hence the value of a nonenhanced scan. degeneration of a benign-appearing neo- plasm suggests a Warthin tumor or pleo- morphic adenoma (41). Perhaps the most useful study that one quired for a definitive diagnosis. Because carotid artery may lead to a preference for can perform to ascertain the nature of a of the precarious position of the facial MR imaging, but bone pain and adenopa- painless mass in the salivary glands is nerve, a core biopsy is generally shunned thy might suggest that CT is the favored image-guided aspiration or biopsy (Fig in sampling parotid masses. It should be modality. 12). The request for image-guided aspira- noted that inflammatory masses of the Some head and neck surgeons do not tions most often arises when a deep lobe salivary glands may mimic epithelial neo- perform any imaging or aspirations prior parotid mass or parapharyngeal space ec- plasms at cytology because desquamated to operating on a salivary gland mass. topic minor salivary gland lesion is inci- cells frequently populate the former. This This is usually in the setting of a superfi- dentally discovered. Since the lesions are is a known potential pitfall of head and cial painless mobile parotid mass with nonpalpable and difficult to approach neck cytology and accounts for many normal facial nerve function (presumed endoscopically, the radiologist may be inaccurate aspiration results (42,43). to be a pleomorphic adenoma). called on to obtain a tissue sample. In those cases in which the diagnosis is Whether or not one chooses to puncture known from a biopsy or aspiration per- the lesion from the anterior face via a formed under palpation guidance, the OBSTRUCTIVE OR retromaxillary (transbuccal) or a transpa- emphasis in imaging should shift toward INFLAMMATORY LESIONS rotid approach depends on the comfort delineation of the size and extent of the level of the radiologist and the course of mass rather than histologic discrimina- Most patients with sialolithiasis (salivary the carotid vessels with respect to the tion. Once again, symptoms may suggest gland calculi) will have the cardinal signs mass. Cytologic aspirates with 22-gauge one modality over another since the pres- of pain and swelling of the gland (44–47). spinal needles are usually sufficient, but ence of cranial nerve palsies, meningeal Sialolithiasis is the second most common occasionally core biopsies of the gland signs, venous obstruction, and fixation of disease of the salivary glands after mumps with 18–20-gauge needles may be re- the mass to vital structures such as the (44). The gland may be diffusely or focally

24 • Radiology • July 2000 Yousem et al sialoliths, the surgeon may decide to treat the patient with resection of the gland. This is often the preferred treatment for patients with recurrent bouts of sialoli- thiasis with sialadenitis, since this region of the duct is not well accessed transor- ally. A cervical (submandibular) surgical approach may be taken with sialoliths that extend beyond the mylohyoid (in the proximal duct). Most of the imaging modalities that are sensitive to calculi, such as conventional radiography, CT (48), and US (49,50), can demonstrate sialoliths with high accu- racy. Of 185 patients with major salivary gland calculi, calculi were identified and localized correctly (intraductal vs intra- glandular) with US in 174 patients (94%) reported in Gritzmann’s review (22). Four- a. c. teen of the 174 cases detected at US were not evident at conventional radiography. However, US is less accurate than CT in distinguishing multiple clusters of stones from single large stones (48,50). Gener- ally, CT in this setting is best performed without administration of contrast mate- rial, since small opacified blood vessels may simulate small sialoliths (Fig 13). If an abscess or inflammatory process is suspected, adding enhanced scans after identifying stones on nonenhanced scans may be useful. Recently, some investigators have advo- cated fast T2-weighted MR imaging with thin sections to noninvasively evaluate the ductal architecture of the salivary glands and to identify stones (Fig 14). b. d. Although beautiful images of the salivary ductal system can be generated with thin- Figure 14. Submandibular calculi visualized at MR imaging. (a) Transverse T1-weighted SE section, T2-weighted MR imaging (51– (500/11) MR image shows two areas of low signal intensity (arrows) in the floor of the mouth on the left. (b) These calculi (arrows) are confirmed on this transverse T2-weighted SE (4,000/80) MR 53), tiny calculi within the gland and image, and the obstructed duct (arrowhead) is evident. Inflammation around the stones accounts even in the larger ductal system can be for some peripheral high signal intensity. (c) The duct (arrowhead) can also be seen on this overlooked on MR images because of the contrast-enhanced, T1-weighted, fat-saturated, spoiled gradient-echo (35/2.1, 30° flip angle) MR signal void associated with the calcified image. The walls enhanced, presumably due to inflammation (). (d) There was stone. Clearly, CT, US, and simple conven- coincidental sialadenitis of the left submandibular gland seen as enlargement and high signal tional radiography will enable identifica- intensity on this transverse, fat-saturated, T2-weighted fast SE (4,000/80) MR image. Note intraglandular ductal dilatation (arrows). tion of the calculi, but MR imaging af- fords the opportunity to visualize the effect the sialolith has on the ductal system. Is this necessary? In most instances, the enlarged with a sialolith in the proximal and may occur within intraglandular duc- answer is no. However, in those cases of a duct. tal tributaries or within the main ducts. painful gland associated with chronic si- Sialolithiasis is predominantly a dis- When in the gland itself, the symptoms aladenitis without a sialolith seen at CT ease of the submandibular gland since may be relatively minor, whereas ductal or conventional radiography, the irregu- 80%–82% (143 of 174) of sialoliths occur sialoliths usually have a more precipitous larity of the ductal system may give a clue here (22,44). Sialoliths form more fre- presentation (44). as to the cause of the painful gland. quently in the submandibular gland be- Ductal calculi may initially be treated Strictures may be present where a sialo- cause of the more alkaline, thicker, and with secretagogues and/or dilation of the lith has resided. The poor outflow of viscous saliva the submandibular gland pro- duct. Transoral resection of sialoliths and leads to chronic sialadenitis. In other cases, duces. Other factors that predispose to sta- sialodochoplasty can be performed for the sialadenitis may not be from calculi sis in the Wharton duct (eg, an uphill isolated distal duct (close to the ampulla) but may be due to autoimmune inflam- course, a dependent gland, a wider lu- sialoliths. Imaging may help define the matory conditions that have a signature men, and a tighter orifice) may play a role location of isolated nonpalpable or mul- sialographic appearance—pruned, trun- as well. Calculi may be multiple (25%) tiple sialoliths. For proximal or glandular cated main ducts with punctate or globu-

Volume 216 • Number 1 Major Salivary Gland Imaging • 25 Figure 15. MR sialography in a healthy volun- teer. The main submandibular duct (arrows) and some of its tributaries (arrowheads) can be seen on this transverse, maximum intensity projection reformatted image from a three- a. b. dimensional, T2-weighted fast SE (5,000/102, one signal acquired) data set. Figure 17. Simple ranula. (a) In the right sublingual gland, the hyperintense lesion (ar- row) on this transverse T2-weighted SE (3,000/ 102) MR image could represent a pleomorphic adenoma or a cyst. (b) The absence of enhance- ment on this fat-saturated, T1-weighted SE (600/17) MR image suggests a cystic lesion, in this case a simple ranula of the sublingual gland. (c) The nonenhancing ranula (curved arrow) lies superior to the geniohyoid muscles (g) and has not perforated through the mylo- hyoid musculature on this coronal T1- weighted SE (600/17) MR image with fat satu- ration.

Figure 16. Acute right-sided parotitis. Trans- verse, contrast-enhanced, fat-saturated, T1- weighted SE (600/30) MR image shows marked c. enhancement of the right parotid gland (thick and thin arrows) compared with the left. The superficial subcutaneous tissue is also inflamed. Can MR sialography replace conven- tional sialography, a cumbersome proce- dure that is contraindicated in patients lar collections peripherally in the glandu- with acute sialadenitis and may result in lar parenchyma (54). The larger ducts are irritation and injury to the duct if not Figure 18. HIV-related lesions. Transverse, spared as the disease affects the periphery performed properly? The answer appears contrast-enhanced CT scan depicts a right- first and spares the central ductal system. to be yes, if not now then very soon (Fig sided parotid cyst (straight arrow) and multiple Tiny abscesses in the glands will show 15). The caveat is that the need to per- small nodules in the left parotid gland (curved similar punctate cystic regions. form sialography should be restricted arrow) in this patient who was HIV positive but Sialography is contraindicated in the to a very few number of cases when had not fulfilled criteria for acquired immuno- acute setting of sialadenitis because of the clinical assessment, serology (especially deficiency syndrome. possibility of exacerbating the symptoms for the autoimmune causes), conven- associated with the infection. The retro- tional radiography, and/or CT cannot fa- grade injection of contrast agents can force cilitate diagnose of the cause of the Other causes of acute parotitis include inflammatory products into the more pe- chronic sialadenitis. viral (mumps), bacterial (staphylococcus ripheral parenchyma of the gland. Fur- Sialolithiasis often causes sialadenitis and streptococcus), granulomatous (tuber- thermore, the act of instrumenting the (44). The inflamed gland will be large and culosis, candida, cat-scratch fever), and duct may irritate it, cause narrowing from painful, and the cardinal signs of warmth postpartum parotitis. Poor dental hy- posttraumatic or stricture forma- and redness may be present over the gland. giene may contribute to the development tion, and lead to reduced drainage of the Secondary involvement of the glands by of affecting the submandibu- infected saliva. MR sialography has the odontogenic abscesses may also lead to lar, sublingual, and parotid glands. The advantage of not requiring cannulation infection of the gland. Purulent material minor salivary glands rarely show inflam- of the duct and a heightened sensitivity may be expressed from the ductal orifice matory change other than mucous reten- to edema in the salivary gland, which in most bacterial infections and is the best tion cysts from local obstruction. may not be evident at CT. clinical sign of an infected gland. If the patient is experiencing his or her

26 • Radiology • July 2000 Yousem et al CT scan, US scan, or conventional radio- graph. Contrast-enhanced CT and MR imaging are currently the best ways to demonstrate a glandular abscess. Because of the fatty attenuation and intensity that is intrinsic to the parotid glands, particularly as one ages, abscesses are particularly well seen on enhanced CT scans and fat-saturated, T1-weighted MR images. CT has been shown to be of benefit Figure 21. Glandular calcifications in a pa- in evaluating the inflammatory masses tient with sarcoidosis. Transverse nonenhanced when compared to MR imaging (55). Figure 19. Sjo¨gren disease. While both parotid CT scan shows the presence of multiple small One should include superinfected HIV- glands (arrowheads) show cystic changes in calcifications in the parotid glands bilaterally. and enlargement of the gland on this coronal related cysts, suppurative parotid lymph T2-weighted SE (4,000/80) MR image, the left nodes, and cystic degeneration of neo- side also shows periparotid adenopathy (ar- plasms with or without superimposed row). This pattern may be seen with Sjo¨gren ing deep cervical fascia with acute infection in the differential diagnosis of disease or HIV-related lymphoepithelial cysts parotitis. This is seen equally well at MR abscesses of the gland. and nodules. imaging and CT. The gland will have high There are a number of manifestations signal intensity at T2-weighted MR imag- of chronic sialadenitis, both clinically ing. The presence of adjacent lymph and radiographically. Most important, the nodes or intraglandular lymph nodes may changes from chronic sialolithiasis may suggest the inflammatory nature of the result in a small atrophic gland with focal lesion but can also be seen, in another intraglandular calcifications. Rarely, one clinical setting, with neoplasms. may see a large ductal stone still remain- CT and MR imaging in the coronal ing with no evidence of acute inflamma- plane for inflammatory conditions of the tion and inducing no pain. This occurs parotid and submandibular glands may most frequently in the submandibular be helpful for evaluating the extent of the gland. lesion. The relationship of the inflamma- A mucous plug in the duct may also tory mass to the floor of the mouth (as cause a painful, swollen gland (Kussmaul with a ranula) for submandibular lesions disease). One pseudomass associated with and the skull base for parotid gland masses calcifications in the gland is termed the has importance with respect to the surgi- ‘‘Kuttner tumor,’’ a focal, masslike firm- cal approach. A ranula has been termed a ness of the submandibular gland due to mucous escape cyst, a mucous retention chronic sialadenitis from sialolithiasis. Figure 20. Conventional sialography. The ex- cyst, and a mucocele of the sublingual tent of the ductal system and its tributaries is gland or neighboring minor salivary glan- well seen on this conventional sialogram in a dular tissue (Fig 17). A ranula that is SYSTEMIC DISORDERS OF THE patient who has Sjo¨gren disease. Note the tiny MAJOR SALIVARY GLANDS areas of cavitation (arrows) in the periphery. superficial to the (a simple ranula, epithelial lined) is usually addressed transorally. It may be treated In the category of systemic disorders that with resection or, in some cases, marsupi- affect the major salivary glands, there are first episode of acute sialadenitis in the alization. The lingual and hypoglossal a number of autoimmune diseases. HIV- setting of dehydration or a palpable sialo- nerves must be carefully identified during related cysts and nodules (Fig 18), Sjo¨gren lith, the otorhinolaryngologist may elect the operation. A ranula that plunges type 1 (previously known as Mikulicz to forego imaging and treat empirically. through the muscular floor (a plunging disease) and Sjo¨gren type 2 (Fig 19), and Surgeons are loath to operate in the set- ranula or pseudocyst, not epithelial lined) sarcoidosis fall within the general rubric ting of acute parotitis. Surgical planes are may be excised through a transcervical of autoimmune disorders with salivary obliterated, and the dissection of the fa- submandibular incision with a neck dis- gland manifestations (56). CT is probably cial nerve is very cumbersome when the section. This allows complete resection of the best way to image patients with sys- surrounding gland is edematous and in- the cyst and will help spare the lingual temic disorders since calculi may be at the flamed. Medical management is indi- and hypoglossal nerve. Alternatively, the root of or a byproduct of the acute symp- cated. Even when an abscess is present, surgeon may excise the sublingual gland toms related to the systemic disorder. most head and neck surgeons prefer to transorally and pack the cyst or place a Sjo¨gren syndrome and sarcoidosis predis- wait until antibiotics have reduced the drain in it. By treating the gland, some pose to stone formation. The attenuation diffuse inflammation in the gland before believe the plunging cyst will resolve on of the gland may be increased with both tackling the focal mass. its own. Sjo¨gren disease and sarcoidosis. Focal On CT or MR images, one may see the Occasionally, one will identify an ab- masses may be present with cysts, nod- inflamed gland as enlarged, of abnormal scess in the gland that is associated with ules, and lymph nodes in all of the dis- attenuation or intensity, and enhancing infiltration of the subcutaneous tissue eases listed above. avidly (Fig 16). There is usually inflamma- and/or the glandular tissue. As always, Sialography may be useful in staging tory stranding into the overlying subcuta- one should exclude a sialolith as the Sjo¨gren syndrome, since patients’ symp- neous tissue and thickening of the invest- cause for the abscess on a nonenhanced toms may not correlate well with severity

Volume 216 • Number 1 Major Salivary Gland Imaging • 27 of the disease (Fig 20). The results of a The disorder is rarely imaged but usually predicting the histology of submandibu- prospective study comparing MR sialogra- shows enlarged parotid glands of in- lar masses with CT or MR imaging. Radiol- ogy 1998; 208:441–446. phy (6,000/115; flip angle, 60°; pixel size, creased attenuation and slightly increased 2. Kane WJ, McCaffrey TV, Olsen KD, Lewis 0.29 ϫ 0.31 ϫ 3 mm) with the standard of T2 intensity. JE. Primary parotid malignancies: a clini- reference conventional sialography showed Granulomatous diseases, including fun- cal and pathologic review. Arch Otolaryn- an agreement rate of 89% (P Ͻ .001) in gal infections, Wegener disease, tubercu- gol Head Neck Surg 1991; 117:307–315. staging the disease (57). For identifying losis, syphilis, and cat-scratch fever, may 3. Batsakis JG. Tumors of the head and neck: clinical and pathological considerations. stage I or greater disease and stage II or produce painless focal or generalized Baltimore, Md: Williams & Wilkins, 1979. greater disease, MR sialography was 100% masses in the salivary glands. If there are 4. Freling NJ, Molenaar WM, Vermey A, et and 91% accurate, respectively (57). Punc- calcifications within a painless mass in al. Malignant parotid tumors: clinical use tate, globular, and destructive patterns the parotid gland, granulomatous dis- of MR imaging and histologic correlation. Radiology 1992; 185:691–696. may be discerned with MR sialography eases and pleomorphic adenoma become 5. Weber RS, Byers RM, Petit B, Wolf P, Ang (58). the most likely diagnoses. Sarcoidosis pre- K, Luna M. Submandibular gland tumors: In most cases, the diagnosis of Sjo¨gren disposes to glandular calcifications (Fig adverse histologic factors and therapeutic disease is made clinically based on the 21) with or without nodes. implications. Arch Otolaryngol Head Neck Surg 1990; 116:1055–1060. sicca syndrome and the connective tissue Unusual disorders such as Kimura dis- 6. Shah JP. Head and neck surgery. 2nd ed. disorder (eg, rheumatoid arthritis) com- ease (eosinophilia, lymphoid prolifera- London, United Kingdom: Mosby-Wolfe, bined with serology of antinuclear anti- tion in neck nodes and salivary glands, 1996; 431–460. bodies. Sialography, be it MR or conven- usually occurring in Asian patients), amy- 7. Weber RS, Palmer JM, el-Naggar A, Mc- Neese MD, Guillamondegui OM, Byers tional, is used primarily to stage disease loidosis, toxoplasmosis, , RM. Minor salivary gland tumors of the (see previous section). For those cases in and hematogenous metastases (usually and buccal mucosa. Laryngoscope which the diagnosis is in question, some from thyroid or renal cell carcinoma) 1989; 99:6–9. would favor performing a lip biopsy of rarely will affect the parotid gland. 8. Schlakman BN, Yousem DM. MR of intra- the minor salivary gland tissue over sialog- The clinical history will usually offer parotid masses. AJNR Am J Neuroradiol 1993; 14:1173–1180. raphy. Still others have suggested that a the best means for establishing that the 9. Parker GD, Harnsberger HR. Clinical- biopsy of the parotid gland has a higher parotid gland is affected by systemic disor- radiologic issues in perineural tumor yield than a labial biopsy since the sensi- ders. Imaging, if required, is used primar- spread of malignant diseases of the extra- tivity for Sjo¨gren disease with labial mi- ily to assess an atypical dominant mass. cranial head and neck. RadioGraphics 1991; 11:383–399. nor salivary gland biopsy is 58% (21 of 36 In this scenario, MR imaging is probably 10. Barakos JA, Dillon WP, Chew WM. Orbit, patients) compared to 100% (36 of 36 the most effective study. skull base, and : contrast-en- patients) for parotid biopsy (59). hanced fat suppression MR imaging. Radi- Sjo¨gren syndrome increases the risk of ology 1991; 179:191–198. 11. Dillon WP. Imaging of central nervous parotid lymphoma by more than 4,400% SUMMARY system tumors. Curr Opin Radiol 1991; (60). Therefore, any dominant mass in a 3:46–50. Sjo¨gren-affected parotid gland must be Most disorders of the salivary glands will 12. Teresi LM, Lufkin RB, Wortham DG, Abe- considered lymphoma and requires aspi- mayor E, Hanafee WN. Parotid masses: manifest a few discrete clinical scenarios. MR imaging. Radiology 1987; 163:405– ration or biopsy with assessment of cellu- Because sialolithiasis may have a variety 409. lar clonality. MR imaging has been particu- of manifestations, CT should be the main- 13. Swartz JD, Rothman MI, Marlowe FI, larly helpful with identifying dominant stay of imaging. Optimal imaging evalua- Berger AS. MR imaging of parotid mass lesions: attempts at histopathologic differ- masses within glands affected by Sjo¨gren tion of the salivary glands may require disease (60). entiation. J Comput Assist Tomogr 1989; nonenhanced (to visualize sialoliths), en- 13:789–796. Som et al (39) have coined the term hanced (to identify abscesses, cysts, and 14. Som PM, Biller HF. High-grade malignan- ‘‘acquired immunodeficiency syndrome– neoplasms), or both nonenhanced and cies of the parotid gland: identification with MR imaging. Radiology 1989; 173: related parotid cysts’’ to describe the cysts enhanced (for painful masses for which associated with HIV infection and note 823–826. one cannot exclude sialolithiasis) CT 15. Sigal R, Monnet O, de Baere T, et al. that they are hard to distinguish from scans. On the other hand, with a sub- Adenoid cystic carcinoma of the head and Sjo¨gren-related benign lymphoepithelial acute manifestation of a nonpainful, non- neck: evaluation with MR imaging and lesions. In patients who are HIV positive, inflammatory mass, where there is a high clinical-pathologic correlation in 27 pa- one can see both cysts or lymphoid nod- tients. Radiology 1992; 184:95–101. degree of suspicion for neoplasm, con- 16. Kaneda T, Minami M, Ozawa K, et al. ules in the parotid glands. Complemen- trast-enhanced, fat-saturated MR imaging Imaging tumors of the minor salivary tary findings of cervical adenopathy, will best demonstrate the extent of dis- glands. Oral Surg Oral Med Oral Pathol adenoidal hypertrophy, and tonsillar en- ease and the presence of perineural seed- Oral Radiol Endod 1994; 78:385–390. largement may also be present (61). 17. Berg HM, Jacobs JB, Kaufman D, Reede ing. Sialography, if indicated at all, may DL. Correlation of fine needle aspiration In addition to the autoimmune disor- be performed with heavily T2-weighted biopsy and CT scanning of parotid masses. ders in the preceding paragraphs, the MR techniques. Laryngoscope 1986; 96:1357–1362. salivary glands may be affected by other 18. Som PM, Shugar JM, Sacher M, Stollman systemic disorders. Sialosis refers to a Acknowledgment: The authors would like to AL, Biller HF. Benign and malignant pa- bilateral, painless enlargement of the sali- acknowledge the kind support provided by rotid pleomorphic adenomas: CT and MR studies. J Comput Assist Tomogr 1988; vary glands that may be caused by sys- Laurie A. Loevner, MD, in the analysis and collection of the images and material presented 12:65–69. temic disorders such as diabetes mellitus, herein. 19. Keyes JW Jr, Harkness BA, Greven KM, alcoholism, hypothyroidism, and malnu- Williams DW, Watson NE Jr, McGuirt WF. trition. 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