14832916 So No Graphic Assessment of the Sub Mandibular Space

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PICTORIAL REVIEW

Sonographic assessment of the submandibular

space

D.C. Howletta,*, F. Alyasa, K.T. Wongb, K. Lewisc, M. Williamsc,A.B. Moodyc, A.T. Ahujab

Received 10 March 2004; received in revised form 1 June 2004; accepted 11 June 2004

KEYWORDSSalivary glands;Submandibular;Pathology;Ultrasound (US)

There is a wide variety of pathological processes which may present with swellingin the submandibular space. Although the submandibular gland is the most importantstructure in this region, there are a number of extraglandular causes of swellingwhich frequently mimic submandibular gland enlargement. In this review the use of

high-resolution ultrasound in the assessment of the submandibular gland andadjacent structures is discussed and illustrated.q 2004 The Royal College of Radiologists. Published by Elsevier Ltd. All rightsreserved.

Introduction

Diseases of the submandibular glands tend topresent clinically as palpable unilateral or bilateral

glandular enlargement that may, or may not, bepainful. It is often difficult to establish on physicalexamination whether swelling relates to the sub-mandibular gland itself or is due to enlargement ofan adjacent structure. The submandibular spaceand its contents are, however, superficial struc-tures and are readily accessible to high-resolutionultrasound examination. In this article the normalsonographic appearances of the submandibularspace are described, with a section on sonographictechnique. The pathological processes that involvethis region are discussed, with particular reference

to those disease entities which may mimic sub-mandibular swelling and can be differentiatedsonographically.

Normal sonographic anatomy of thesubmandibular space

The submandibular space lies inferolateral to themylohyoid muscle and is bordered by the hyoid boneinferiorly. Posteriorly there is free communicationbetween the submandibular space and the sublin-gual space (which lies superomedial to the mylo-hyoid). Large sublingual lesions can extend into thesubmandibular space and present as a submandib-ular swelling.

The principal component of the submandibularspace is the submandibular gland. Although there isno formal anatomical division of the gland it is, byconvention, divided into superficial and deeplobes.1 The gland has a U-shape and wraps around

the mylohyoid muscle, with the superficial lobeinferolateral to the mylohyoid, running parallel tothe anterior belly of the digastric muscle. The deeplobe, which contains the gland hilum, lies super-omedial to the mylohyoid.2 For practical purposeshowever, the distinction between superficial anddeep lobes is not important, because surgicalapproaches treat the gland as a whole.

Sonographically, the gland is encapsulated and ofhomogeneous echotexture, not dissimilar inappearance to the parotid gland. Intraglandular

Clinical Radiology (2004) 59, 1070–1078

0009-9260/$ - see front matter q 2004 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.doi:10.1016/j.crad.2004.06.025

* Guarantor and correspondent: D. C. Howlett, Department ofRadiology, Eastbourne District General Hospital, Kings Drive,Eastbourne BN21 2UD, UK. Tel.: C44-1323-417400; fax: C44-1323-414933.

E-mail address: [email protected] (D.C. Howlett).



ducts are seen as linear, hyperechoic structures(Fig. 1). Wharton’s duct emerges from the glandhilum and passes medially around the mylohyoid,medial to the sublingual gland, and advancesmedially to the papilla in the floor of the mouthat the base of the frenulum.3 Although Wharton’s

duct is best seen when pathologically dilated, itmay be seen in normal subjects (Fig. 2), as a thin-walled, tubular structure. Normal lymph nodes arenot found within the submandibular glands, unlikethe parotids, owing to early glandular encapsulation.

The submandibular gland has some importantvascular landmarks nearby. The facial artery andvein pass lateral to the gland in the submandibularspace, with the lingular artery and vein crossingover the mylohyoid, medial to the deep lobe of thegland. It can be helpful also to identify the anteriorbranch of the retromandibular vein where it passes

between the anteroinferior parotid and the dorsalsubmandibular gland.3 This vessel may be displacedby an adjacent salivary gland mass, giving an idea oflesion origin depending on direction of vesseldisplacement.

Other contents of the submandibular spaceinclude fat, the inferior loop of the hypoglossalnerve and regional lymph nodes (submandibular andsubmental). The submandibular gland can beseparated from the adjacent parotid gland by theinterposition of the superior digastric lymph node,Kuttner’s node (Fig. 3), but the two glands may

appear in continuity.4

Sonographic technique

The submandibular space is interrogated sonogra-phically in transverse (axial), oblique axial andlongitudinal planes. Subjects are best imaged lyingwith the neck extended and turned away from theside being examined. Both sides should be routinelyevaluated and, depending on initial sonographicfindings, regional cervical nodes and also the

parotid glands should also be assessed. High-resolution transducers provide the best detail. Airbubbles on the floor of the mouth can simulatecalculi.3

Figure 3 Transverse sonogram to demonstrateKuttner’s node (arrow) separating the posterior aspectof the right submandibular gland (S) from theadjacent parotid (P).

Figure 2 Oblique transverse section through the leftsubmandibular gland which demonstrates a normalWharton’s duct (small white arrows) emerging from the

gland hilum to curve around the mylohyoid (large whitearrow).

Figure 1 Transverse sonogram of the right submandib-ular gland. Note relations of the gland to the mylohyoid(M), hyoglossus (H) and digastric (posterior belly) (D)muscles. The facial vessels are also indicated (large whitearrows). A hyperechoic linear structure within the gland(small white arrow) represents an intraglandular duct.

Sonographic assessment of the submandibular space 1071



Sonographic sssessment of submandibular gland pathology

Sialolithiasis

Between 80 and 90% of salivary gland calculi occur

in the submandibular glands, because of the highermucus content of saliva produced by these glands,and calculi are multiple in up to 25% of cases.5 Mostcalculi occur in Wharton’s duct and only 15% in thegland itself (Fig. 4).1 The turn of the duct aroundthe mylohyoid is a frequent site of calculusimpaction, and duct dilation proximal to anobstructing calculus may be evident (Fig. 5). Calculiare typically hyperechoic foci with distal acousticshadowing. Ultrasound has a reported accuracy ofup to 96% in calculus detection6 and is the initialchoice for investigation of suspected sialolithiasis.

Stones impacted at the duct ostium in the floor ofthe mouth may not be well seen sonographically.

Acute sialadenitis

Acute submandibular sialadenitis presents withpainful glandular swelling, and there may beassociated regional adenopathy. Viruses, in par-ticular mumps, are the commonest cause ofsialadenitis. Patients with decreased saliva pro-duction (secondary to dehydration, duct strictureor calculus) are prone to bacterial sepsis; Staphy-

lococcus aureus is the most commonly isolatedorganism.3 Abscess formation may occur in severecases. Tuberculosis, histoplasmosis or actinomyco-sis may cause granulomatous sialadenitis, but theseconditions are rare.

Sonographically, the acutely inflamed gland

appears enlarged and hypoechoic and there maybe coarsening of gland texture with evidence ofhypervascularity on colour Doppler examination.Enlarged adjacent nodes are often apparent (Fig.6). Ultrasound is useful also if abscess formation issuspected clinically, and can be used to aspiratefluid collections.

Chronic inflammatory conditions

Recurrent bouts of infective sialadenitis, oftensecondary to duct stricture or calculus, may causeprogressive glandular damage and finally atrophy.

Figure 4 Longitudinal sonogram through the left sub-mandibular gland demonstrates multiple intraglandularhyperechoic calculi, with prominent dense distal acousticshadowing.

Figure 5 Sonogram of the right submandibular gland inthe same patient as Fig. 4 demonstrates gross intragland-

ular sialectasis secondary to a longstanding obstructingduct calculus. Note normal gland peripherally (whitearrow).

Figure 6 Transverse sonogram of the right submandib-ular gland in acute sialadenitis. The gland is enlarged andhypoechoic with coarsening of the texture apparent. Noteenlarged, adjacent reactive lymph node.

D.C. Howlett et al.1072





ultrasound is used for gland surveillance. Personswith suspected Sjogren’s syndrome should also havetheir lacrimal glands examined sonographically forevidence of disease involvement, which is common(Fig. 13).

(b) Sarcoidosis

Sarcoidosis involves the parotid glands in 6% ofpatients Submandibular involvement is less com-mon and may present as a painless lump. Thesonographic features are non-specific but tend to

demonstrate a coarse and hypoechoic gland whichis normal in size or enlarged (Fig. 14). Core biopsymay confirm infiltration with sarcoid granulomataand obviate the need for surgical excision.

Submandibular gland tumours

Submandibular gland tumours usually present withpain or a palpable lump. Ultrasound is useful for theevaluation of suspected submandibular tumour; it

can demonstrate whether a lesion is intra- orextraglandular, is able to characterize lesions andcan also demonstrate associated adenopathy. Up to20% of masses thought clinically to originate fromthe salivary gland may be demonstrated sonogra-phically to be extraglandular.9 There is anincreased incidence of malignancy (approximately50%) in submandibular tumours3 when comparedwith the parotids (10%). Ultrasound can alsoindicate the need for further imaging (CT or MR),particularly for large or atypical lesions, whoselocal extent or nature is difficult to assess

sonographically.

Benign tumours

The vast majority of benign submandibular neo-plasms are pleomorphic adenomas.7 Sonographi-cally they have features similar to those describedin the parotids, being rounded, circumscribed andhypoechoic, with distal acoustic enhancement (Fig.15).10 Larger lesions may develop more atypicalfeatures, with a heterogeneous internal architec-ture, cystic changes and loss of clarity of margins10

and may mimic malignancy. Longstanding tumours

Figure 10 Sonogram of the submandibular gland in apatient with relatively advanced Sjogren’s syndrome. Thegland is hypoechoic, with a coarse, reticulated echo-

pattern, and internal hypoechoic foci are present.

Figure 11 Advanced Sjogren’s syndrome with a promi-nent multicystic pattern of involvement is demonstratedin this submandibular sonogram. The cysts are due tointraglandular sialectatic changes. A similar appearancemay occur in HIV infection.

Figure 12 Sonogram of the right submandibular glandin a patient with longstanding Sjogren’s syndrome. Ahypoechoic mass is present within the gland (callipers)and there is associated distal acoustic enhancement.Biopsy confirmed involvement with B cell lymphoma.




may calcify and are at risk of malignant degener-ation. Colour Doppler findings vary, but a peripheral“basket-like” pattern of flow may be seen.11

Ultrasound-guided fine-needle aspiration or corebiopsy may be used to establish a diagnosis.

Oncocytoma is a rare salivary gland neoplasmwith sonographic appearances similar to those of

pleomorphic adenoma.10

Warthin’s tumour arisesfrom heterotopic salivary gland tissue in

intraparotid lymph nodes and occurs almost exclu-sively within the parotid glands.

Haemangiomas of the submandibular gland tendto appear in children and may be associated withblue discoloration of the overlying skin. Sonogra-phically, they appear poorly defined and inhomo-geneous, and internal vascular spaces and calcifiedphleboliths may be apparent (Fig. 16). Colour flowin vessels is sluggish however, and may be difficult

Figure 15 Sonogram of a submandibular gland pleo-morphic adenoma. This lesion appears circumscribed,

hypoechoic and homogeneous with associated distalacoustic enhancement.

Figure 16 Sonogram of a haemangioma involving thesubmandibular gland in a 9-year-old boy. The mass ispoorly-defined and of heterogeneous echotexture. Vas-cular spaces are present (small white arrows) as is acalcified phlebolith (large white arrow).

Figure 14 Sonogram of the right submandibular glandof a patient with sarcoidosis proven at submandibularbiopsy. The gland is hypoechoic with a coarse echotex-t ure. T he parot id g land s were als o invol ve dsonographically.

Figure 13 Axial sonogram of an abnormal right lacrimalgland (arrow) in a patient with Sjogren’s syndrome. Thegland is enlarged with a lobulated margin, and containssmall hypoechoic foci. The sonographic appearances arenot dissimilar to those demonstrated in Fig. 10.




to demonstrate sonographically. Haemangiomasare frequently compressible and may change insize with the Valsalva manoeuvre or crying.3

Malignant tumours

Primary malignant submandibular gland tumours

are relatively more common than in the parotidglands. Ultrasound alone may predict malignancy inup to 89% of cases,12 although the various forms ofmalignancy cannot be differentiated.10 Adenoidcystic carcinoma is the commonest malignant sub-type, and the ultrasound features may depend onthe grade of tumour.10 Low-grade, small lesions canappear well defined and not dissimilar to pleo-morphic adenoma. Larger lesions develop moreovertly malignant features, including irregular andpoorly defined margins, heterogeneous internalarchitecture (Fig. 17) and increased resistive

index on colour Doppler assessment.

10

Mucoepider-moid cyst, acinic cells and adenocarcinoma mayhave similar features. Extraglandular spread oftumour can be detected sonographically (Fig. 18)and the neck should be assessed for malignantadenopathy. Adenoid cystic carcinoma has a ten-dency to perineural and perivascular spread and isbest further assessed with MR. The submandibularglands may also be involved by haematogenousmetastases (often head and neck, breast or lungcarcinoma or melanoma) or by lymphoma. Aspreviously mentioned, primary glandular lymphomamay occur in Sjogren’s syndrome but otherwise

involvement is usually haematogenous, because theglands do not normally contain lymphoid tissue.

Other lesions of the submandibular space

Several other pathological processes can involvethe submandibular space and mimic lesions of thesubmandibular gland. Ultrasound can usuallyreadily identify their extraglandular situation andcharacterize their nature.

Figure 17 Sonogram demonstrating adenoid cysticcarcinoma of the submandibular gland. There is a poorlydefined, hypoechoic intraglandular mass present. Notedistal acoustic shadowing.

Figure 18 Sonogram of mucoepidermoid carcinoma ofthe submandibular gland. A poorly defined mass is

present, which is hypoechoic, and there are some flecksof internal calcification. Note extracapsular extension oftumour (arrow).

Figure 19 An enlarged, lobulated node is presentclosely adjacent to the right submandibular gland (S).The node has a hyperechoic central hilum but the cortexis heterogeneous and contains hypoechoic nodules(arrows). Excision confirmed toxoplasmosis involvement.




Adenopathy

The submandibular space is a common site foradenopathy of whatever cause. Nodal involvementby carcinoma or lymphoma may be identified, withnodes becoming rounded and replaced by tumourwith loss of normal hilar echo pattern;7 normalnodes have a typical sonographic appearance.10 Fig.

19 shows other, more unusual causes ofadenopathy.

Second branchial cleft cyst

These embryological remnants usually lie at theangle of the mandible along the anterior border ofthe sternocleidomastoid muscle and can mimicsubmandibular gland lesions when enlarged, par-ticularly if they become infected.7 Sonographicfeatures are variable: lesions tend to be well-defined but may appear echo-poor, mixed cysticand solid, or pseudo-solid (Fig. 20).

Ranula

A ranula is a mucous retention cyst of the sublingualgland. A simple ranula appears as a cyst in the floorof the mouth. A diving ranula can pass into thesubmandibular space and present as a submandib-ular mass. The lesion can often be characterizedsonographically, demonstrating its extension fromthe sublingular space (Fig. 21(a) and (b)).

Parotid lesions

As previously mentioned, lesions of the parotidgland can closely abut the submandibular gland and

mimic a submandibular lesion clinically (Fig. 22).Ultrasound and fine-needle aspiration or corebiopsy will usually confirm the parotid origin of amass pre-operatively and hence help avoid poten-tial facial nerve injury.

Figure 21 (a) Longitudinal sonograms of the right

submandibular space at the upper pole and (b) lowerpole of the submandibular gland showing a diving ranulaas a lobulated cystic mass (arrows) containing internalechoes. This can be seen extending posteroinferiorlyfrom the sublingual space (arrows) and passing deep tothe submandibular gland (S), to present with swelling atthe gland’s lower pole.

Figure 20 Axial sonogram of a second branchial cleftcyst (B) with a pseudo-solid appearance adjacent to theleft submandibular gland lateral aspect (S).




Lipomas

These arise from extraglandular fat usually, butmay present as a submandibular gland lesion.Sonographically they appear as compressible,oval, circumscribed masses with typical striped orfeathered internal echotexture (Fig. 23).10 They donot usually contain internal flow on colour Dopplerexamination.11

Conclusion

Ultrasound represents the initial imaging techniqueof choice for assessment of palpable abnormalitiesof the submandibular gland and adjacent structureswithin the submandibular space. Ultrasound is ableto classify lesions as intra- or extraglandular andcan characterize abnormalities, acting also as aguide for further imaging. It is particularly helpfulin the assessment of suspected sialolithiasis orsubmandibular abscess and can be used to direct

fine-needle aspiration or core biopsy of suspiciouslesions. Ultrasound will answer most clinical ques-tions and can provide important pre-operativeinformation.

Acknowledgements

The authors would like to thank Nick Taylor for

preparation of the illustrations and Louise Pellettfor the preparation of the manuscript.

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Figure 22 A Warthin’s tumour arising from the infer-omedial left parotid gland (P) is seen sonographically as a

complex, hypoechoic mass (arrow). This closely abuts theadjacent submandibular gland (S) and could be confusedclinically with a submandibular lesion.

Figure 23 Sonogram to include the lower pole of theright submandibular gland (S) demonstrates an elliptical,circumscribed hypoechoic mass with internal stripedhyperechogenicity. This lesion is separate from thegland and is consistent with a lipoma.


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14832916 So No Graphic Assessment of the Sub Mandibular Space