Sonography of Salivary Gland Tumors and Disorders

Abstract

Diseases of the salivary glands are as common as they are diverse and can have different causes. Clinicians can differentiate salivary gland changes based on chronic systemic diseases, congenital and vascular malformations, and benign and malignant tumors. Acute infectious pathologies can also arise as a result of obstructive pathologies. A large number of diseases with similar clinical presentations have to be differentiated. Due to the improved resolution of ultrasound technology over the last 20 years, it is now used as the first imaging modality to examine salivary gland pathologies. It allows a quick, dynamic, and non-invasive examination of the salivary glands and the soft tissue of the neck. In order to accurately diagnose and treat patients, a very good knowledge of these diseases and their appearance on sonography is required.

 

MissingLinkText

Keywords

Speicheldrüsen - Sialadenitis - Sialolithiasis - Pleomorphes Adenom - Warthin Tumor

Objectives

This article is intended to help readers for the following:

• to gain an overview of the many possible disorders of the salivary glands, as well as the most important acute and chronic pathologies of the salivary glands,

• to differentiate benign from malignant tumors using sonography,

• to diagnose rare chronic or immunological diseases and sialadenoses,

• to understand the advantages and disadvantages of ultrasound technology, including contrast-enhanced US (CEUS), color-coded duplex sonography (CCDS), and elastography, and to learn about their value in examination of salivary gland disorders.

Patient consent was obtained for photo documentation.

 

MissingLinkText

Introduction

A 45-year-old patient presents at our outpatient clinic with an asymmetrical pre-auricular swelling on both sides that has been present for a few days for further investigation. He has a feeling of tension but no severe pain. When asked about a connection with food intake, the patient denies any connection. This is a first-time occurrence and in addition to the symptoms described, the patient notices swelling of both upper eyelids and complains of slightly delayed dryness of the mouth and eyes. There are no relevant co-morbidities, and he is protected by vaccinations in line with the recommendations of the Standing Committee on Vaccination; there are no noxious agents, and the patient has never had surgery in the head and neck area.

Various diseases can explain the described symptoms of swelling in the head and neck area – alongside clinical examination, sonography plays an important role in further clarification. The presentation and causes of salivary gland disorders vary and require the support of relevant diagnostic tools to treat patients successfully. In addition, the causes and manifestations of this disorder are different in children than in older patients. This article aims to provide an overview of the relevant salivary gland disorders and the associated changes in sonography.

Excursus: Standardized ultrasound examination of the salivary glands

Sonography of the salivary glands is typically performed with an ultrasound transducer using a frequency between 5–13 MHz and should always start on the non-pathological side. Compared to muscle, normal salivary gland tissue is hyperechoic and has a slightly granular and homogeneous texture.

Generally, an ultrasound examination of the sublingual glands will be performed from the submental side ([Fig. 1]). In the submental transverse plane, you will see the “Mickey Mouse” formation that includes the anterior belly of the digastric muscle (MD), the mylohyoid muscle (MMH), the sublingual glands (GSL), the geniohyoid muscle (MGH), and the genioglossus muscle (MGG).

Fig. 1 Transversal plane examination of the sublingual gland.

The submandibular gland is best visualized within the submandibular triangle in a longitudinal plane ([Fig. 2]). From this angle, the mylohyoid muscle (MMH) can be seen, which appears hypoechoic compared to the submandibular gland.

Fig. 2 The longitudinal view of the submandibular gland. Mylohyoid muscles (Musculus mylohyoideus: MMH); submandibular gland (Glandula submandibularis: GSM), parotid gland (Glandula parotis: GLP), root of the tongue (ZG).

The parotid gland ([Fig. 3] and [Fig. 4]) should be examined in 2 steps: from below the mandible in a transverse plane to visualize the caudal parotid gland, and above the mandible additionally in a vertical plane. Dorsal to the mandible, the retromandibular vein can be seen in the Doppler examination, which represents a landmark for the anticipated course of the facial nerve. This can be helpful, for example, in preoperative planning.

Fig. 3 Images of the caudal parotid gland (GLP), digastric muscle, posterior belly (Musculus digastricus venter posterior: MDVP), mandible (UK), and masseter muscle (MM).

Fig. 4 Doppler imaging of the retromandibular vein (Vena retromandibularis: VRM). Sternocleidomastoid muscle (Musculus sternocleidomastoideus: MSCM), parotid gland (GLP), digastric muscle (Musculus Digastricus: MDV).

[Table 1] provides a list of relevant anatomical landmarks for sonographic examination of the salivary glands.

Table 1 Relevant anatomical landmarks of the major salivary glands.

Sublingual gland	Submandibular gland	Parotid gland
Digastric muscle	Digastric muscle	Digastric muscle
Mylohyoid muscle	Mylohyoid muscle	Retromandibular vein
Inner muscles of the tongue	Inner muscles of the tongue	Sternocleidomastoid muscle
Genioglossus muscle	Root of the tongue	Mandible
Geniohyoid muscle		Masseter muscle

 

MissingLinkText

 

MissingLinkText

Malformations and pediatric diseases

In specialist practice, disorders of the salivary glands are not uncommon in children, but the incidences are significantly lower in pediatric patients than in older patients. The main causes in children are infections, inflammation, and vascular malformations [1]. Congenital anomalies include malformations of the branchial arches and ear tubercles. Pretragal sinus and cysts are usually superficial, and their extent can be easily described sonographically with multi-frequency transducers in relation to the glandular tissue. These changes, which can be easily excised surgically, have to be differentiated from malformations of the first branchial arch region. This is a useful step because the external auditory canal, the parotid gland, and cervicofacial neck soft tissues can be impacted to varying degrees [2].

Agenesis, hypoplasia, or aplasia of the salivary glands are rare but are frequently described in patients with Down syndrome or Treacher Collins syndrome, sometimes in combination with aplasia of the lacrimal gland, and these disorders are typically associated with sicca symptoms. In such cases, the salivary glands may be completely absent or only unilaterally developed, which underscores the importance of bilateral ultrasound examination [3].

Cystic changes and vascular anomalies

Cysts appear sonographically as echo-free, clearly defined space-occupying lesions with dorsal acoustic enhancement. Symptomatically, these can occasionally be perceived as unpleasant, and they can also fluctuate in size. The exact prevalence is not known, as they usually do not cause any complaints. Cysts are usually observed in the context of other diseases, such as Sjögren’s syndrome or juvenile recurrent parotitis.

80 % of hemangiomas in children are observed in the parotid gland, the remaining 20 % are mostly located in the submandibular region and to a lesser extent in the minor salivary glands. In sonographic imaging ([Fig. 5]), these are well-vascularized, often palpably soft space-occupying lesions, which – depending on their arterial and venous composition – can be classified reliably using color-coded duplex sonography [1] [4]. Without evidence of intralesional vessels, the lymphatic malformations form a separate entity. From a sonographic perspective, this is characterized by lobulated, echo-free soft changes that show distal acoustic enhancement ([Fig. 6] and [Fig. 7]). In many cases of macrocystic lesions, sonographically guided puncture and sclerotherapy under sedation are recommended in addition to surgical excision [5].

Fig. 5 Hemangioma of the parotid gland (GP) in longitudinal view: Intraparenchymal on the right, a sharply demarcated hypoechoic space-occupying lesion (RF) with echo-inhomogeneous content is visible in the B-scan image. Color-coded duplex sonography confirms the presence of an intraglandular hemangioma with arterial-venous vascular components.

Fig. 6 Lymphangioma of the left axial parotid gland: 2-year-old male patient with increasing soft swelling of the left cheek and submandibular region. The B-scan image with additional color-coded duplex sonography shows the typical picture of a lymphatic malformation. Three months after sonographically guided sclerosis with Picibanil (right image), a significant volume reduction can be observed.

Fig. 7 Lymphangioma with Doppler imaging. Visualization of a lymphangioma incl. Doppler imaging in the area of the submandibular gland.

 

MissingLinkText

Solid tumors

In addition to hemangiomas, mixed, benign tumors represent 20 % of all space-occupying lesions of the salivary glands in children. Similar to adults, pleomorphic adenomas are described as one of the most common benign tumors in children. Nevertheless, tumors in children are more frequently malignant than tumors in adults [6]. Salivary gland carcinomas in childhood are rare, but they represent a heterogeneous collective similar to those found in adults. Their incidence is reported to be 0.8:1 000 000 and they typically develop around the age of 15 years [7]. Malignant tumors in children have a narrower range of histological entities and show a different biological behaviour than in the adult population, with children having a better long-term prognosis (survival over 90 % after 10 years) [6] [8]. Mucoepidermoid carcinoma accounts for about 50 % of all malignant tumors, followed by acinar cell carcinoma (25–35 %), adenocarcinoma, and adenoid cystic carcinoma. In addition, lymphomas, sarcomas, and neuroblastomas are observed [6] [9]. Mucoepidermoid carcinoma is reported to be the most common malignant entity, and in the presence of a solid salivary gland tumor, the risk of malignancy is increased more than twofold in children compared to the adult population [10].

 

MissingLinkText

Inflammatory changes

In the group of pediatric patients, mumps (formerly called epidemic parotitis) and juvenile recurrent parotitis are the most common inflammatory changes. However, reliable epidemiological data are not available [11]. Infection with paramyxovirus usually results in unilateral or – staggered – bilateral swelling of the parotid glands. In addition to the enlargement of the affected gland, the otherwise normally hyperechoic gland parenchyma is heterogeneously hypoechoic. With symptomatic anti-inflammatory therapy and supportive fluid administration, the clinical and sonographic changes regress after a few days. Other viral forms of sialadenitis (Epstein-Barr virus, cytomegalovirus, or HIV) have a similar sonographic appearance. The second most common cause of sialadenitis is non-obstructive and non-purulent recurrent juvenile sialadenitis. Sonography reveals enlargement and hypoechoic loosening of the gland parenchyma with sialectasis ([Fig. 8]). The course of the disease is often self-limiting once puberty begins. In the acute interval, in addition to analgesics, saliva stimulants, and antibiotics, successful remissions are achieved with sialendoscopy and irrigation with glucocorticoid-containing solutions [12] [13] [14].

Fig. 8 Chronic recurrent juvenile parotitis. Parotid region axial bilateral. The bilateral swelling of the parotid glands (GP) with the typical patchy hypoechoic tissue texture calls to mind a “honeycomb” or “leopard skin” pattern. Within the enlarged gland, segmentally visible glandular ducts are visualized as echo-free, band-like structures.

Compared to the adult population, obstructive sialadenitis in children occurs only sporadically and does not differ from the clinical and sonomorphological findings in adults. In addition to atypical mycobacteriosis, actinomycosis is also a special form of infectious sialadenitis. Atypical mycobacteriosis (MOTT) is usually an infection with the Mycobacterium avium complex. The main age of onset is at the age of 1 to 5 years. The present lymphadenopathy of the facial and neck soft tissues also includes the salivary glands. Redness and swelling of the affected areas may be followed by abscess formation and cutaneous fistula. From a sonographic perspective, the polycyclic intraglandular and paraglandular lymph nodes are enlarged and show intranodal necrosis with abscess lines. Echo-dense calcifications in the lymph nodes or paranodal region are also characterized by hyperechoic-to-hyperechoic acoustic phenomena.

Actinomycosis caused by the gram-positive Actinomyces israelii and Actinomyces gerencseriae can have similar clinical symptoms. Sonography shows induration with redness and swelling of the soft tissues of the neck and adjacent salivary glands [15] [16]. The course of therapy can also be monitored using high-resolution duplex sonography and multi-frequency transducers [13].

 

MissingLinkText

 

MissingLinkText

Acute inflammatory disorders

In children, acute salivary gland inflammation is most often caused by pre-auricular fistulas or juvenile recurrent parotitis [1]. In elderly patients, it is usually accompanied by a lack of fluid intake. The exact prevalence is not known, but the incidence of acute suppurative parotitis is reported to be 0.01–0.02 % of all hospital admissions.

Acute sialadenitis usually has a viral or bacterial cause and manifests itself with sudden pain and swelling of the affected gland. The role of imaging is to differentiate simple inflammation from abscess formation and to discover possible causes of acute infection. These can be obstructive disorders such as sialolithiasis, as well as tumorous diseases such as infected Warthin tumors [17].

Acute sialadenitis usually presents sonographically with significant enlargement and inhomogeneous visualization of the parenchyma in the B-mode image. Color Doppler sonography shows hypervascularization of the gland, and elastography usually shows the parenchyma with inhomogeneous, moderate hardening. From a sonographic perspective, viral and bacterial sialadenitis cannot be distinguished. A purulent secretion with corresponding laboratory findings indicates a bacterial cause.

Another very important function of imaging in salivary gland inflammation is the ability to exclude abscess formation. Sonographically, an abscess presents as a hypoechoic to echo-free, inhomogeneous region with blurred edges. The entire gland shows the typical picture of sialadenitis. Color Doppler sonography shows no vascularization in the colliquation, but increased vascularization of the surrounding inflamed gland. Elastography usually shows a hardened periphery with an unmeasurable region in the center of the lesion (elastography cannot show fluids). Contrast-enhanced sonography could provide further differential diagnostic assistance. In the event of abscess formation, there is a complete absence of perfusion signals [18]. B-mode sonography also provides very important anatomical information, which is important for a low-complication abscess incision or puncture [19].

A difficult differential diagnostic situation can arise in acutely infected Warthin tumors. In such cases, sonographic differentiation from parotid abscess is often problematic, since infected Warthin tumors can also present with blurred margins [19]. Color Doppler sonography can be helpful in such cases, as it can demonstrate intralesional vascularization. In addition, elastography can be very helpful, because it shows the lesion as moderately to severely hardened. Acute sialadenitis or abscesses are often accompanied by cervical lymphadenitis, which can be evaluated sonographically. Finally, the success of treatment can also be monitored in the short-term using sonography.

 

MissingLinkText

Obstructive salivary gland disorders

Sialolithiasis

Salivary stones are the most common cause of obstructive salivary gland disorders (60–70 %) [20] [21] and the main cause of unilateral swelling of the major salivary glands [22]. The pathomechanism is still unclear, but reduced salivation, a change in the pH of saliva, and its composition are described [21] [23] [24] [25]. The submandibular gland is most frequently affected, occurring in 60–95 % of cases [22] [23] [26]. This distribution is mainly explained by anatomical and physiological conditions. Many patients are asymptomatic and only later develop typical food-dependent swelling. Ascending infections can lead to recurrent inflammation of the salivary gland [27] [28] and, if the gland duct system remains obstructed, usually take a chronic course [24].

 

MissingLinkText

Stenoses

With 15–25 % of cases, stenosis is the second most common obstructive disorder of the major salivary glands [29] [30], and the parotid gland is most frequently affected [29] [31]. In one third of the cases, there are several stenoses in one duct system [30]. The causes are varied and include chronic inflammation of the salivary gland and the duct system, as well as autoimmune processes or radioiodine therapy [22] [24] [32]. However, they also occur as congenital changes [32] or as a result of traumatic damage to the duct epithelium [33] [34]. Recurrent swelling and pain, possibly with acute sialadenitis, are typical symptoms and can lead to a degenerative, fibrotic transformation of the salivary gland tissue [28] [30] [31].

 

MissingLinkText

Sonography for obstructive salivary gland disorders

Ultrasound examination is currently considered the diagnostic tool of choice for disorders of the major salivary glands [35], as it promises the highest diagnostic accuracy compared to other imaging procedures [27]. Sonography reveals a hyperechoic reflex along the duct with distal acoustic cancellation and possibly duct ectasia. Further advantages include the rapid, non-invasive, cost-effective, user- and patient-friendly examination [20] [28].

 

MissingLinkText

Minimally invasive therapeutic approaches for sialolithiasis

Asymptomatic sialolithiasis does not require treatment. Whereas sialoliths, or salivary stones, that cause discomfort should be removed [20]. The location, size, number, and mobility of salivary stones are important factors when deciding on the treatment method [20] [36]. Conservative therapy initially includes sialogogues, gland massage, and, in case of acute sialadenitis, possibly antibiotics. Minimally invasive treatment procedures such as duct slitting, diagnostic sialendoscopy, or extracorporeal shock wave lithotripsy enable gland-preserving therapy in 97 % of cases [36].

 

MissingLinkText

Therapeutic approaches for stenoses

In recent years, new minimally invasive methods have become established for the treatment of symptomatic ductal stenoses or strictures of the major salivary glands, most notably interventional sialendoscopy, which has a success rate of 85–90 % [29].

 

MissingLinkText

 

MissingLinkText

Chronic sialadenitis and sialadenoses

Chronic recurrent parotitis of adults

Chronic recurrent parotitis in adults typically presents as recurrent, unilateral, painful swelling of the parotid gland. The adult counterpart of juvenile parotitis usually occurs between the ages of 40 and 60 [37] [38]. The etiology of this chronic inflammation is unclear. One theory describes a reduced saliva production, which leads to a reduced lavage of the salivary gland. Recurrent infections can lead to ductal injuries through the release of inflammatory chemokines. The synchronous formation of microcalculi through the crystallization of bacterial and epithelial waste products may also play a role [25] [39].

 

MissingLinkText

Systemic autoimmune disorders

Sjögren syndrome

Sjögren’s syndrome is the second most common rheumatic disease after rheumatoid arthritis. In addition, it is the most common rheumatic disease in the ear, nose, and throat region. The incidence worldwide is approximately 61 per 100 000 people. In Germany, the prevalence is about 0.4 % [40].

From a pathohistological perspective, this autoimmune disease is described by a lymphocytic infiltration of exocrine glands [41]. In this case, a parenchymal change with progressive damage to the head and neck glands is observed, which leads, for example, to reduced saliva secretion, among other things. The parotid glands are affected most heavily. The main symptom of this disorder are persistent sicca symptoms, which means dry mouth and eyes. Other common symptoms include fatigue, tiredness, joint and muscle pain, and recurring painful swelling of the glands in the head and neck area. In very rare cases, other organs may also be affected.

When typical sonographic changes occur, sonography is sensitive, even if it is not part of the current classification criteria. Studies have shown that the use of an ultrasound scoring system has a higher agreement with the diagnosis of Sjögren’s syndrome compared to scintigraphy as well as biopsy [42] [43] [44] [45] [46] [47] [48]. In a prospective study, it was shown that 5 parameters are suitable for diagnosis: heterogeneous parenchyma, hypoechoic changes within the salivary gland or the “leopard skin” pattern, hyperechoic bands, cystic lesions, calcifications, and atrophy of the salivary gland [44]. When using Virtual Touch Quantification (VTQ), higher values were observed in patients with Sjögren’s syndrome [49] [50].

Regular ultrasound examinations are recommended in patients with Sjögren’s syndrome due to the risk of mucosa associated lymphoid tissue (MALT) lymphoma. This usually presents as a unilateral, painless mass. Sonography reveals a poorly defined, pseudocystic, hypoechoic space-occupying lesion with a honeycomb-like pattern (“cobblestone” pattern) ([Fig. 9]). Increased vascularity is also observed in hypoechoic areas [51] [52].

Fig. 9 MALT lymphoma in known Sjögren’s syndrome.

 

MissingLinkText

Sarcoidosis

Sarcoidosis is a systemic inflammatory disorder of unknown origin that can affect multiple organ systems. At the time of diagnosis, salivary gland involvement is observed in approximately 35 % of patients [53]. Heerfordt syndrome describes a sarcoidosis-associated swelling of the salivary glands with concomitant uveitis and peripheral facial paralysis. In sonographic examination, the salivary glands may appear loose and heterogeneous ([Fig. 10]) [54].

Fig. 10 Sarcoidosis of the parotid gland.

 

MissingLinkText

 

MissingLinkText

IgG4-associated disorders

The name “IgG4-associated diseases” refers to a group of diseases with similar clinical features. There is an increased infiltration of IgG4-positive plasma cells in various organs, which subsequently leads to swelling and loss of function. Involvement of the salivary glands is observed in approximately 25–53 % of patients with IgG4-associated diseases [55].

Swelling is usually bilateral and painless. The submandibular glands are most commonly affected, but the parotid, sublingual, or lacrimal glands may also be affected. Mikulicz syndrome describes involvement of all of the aforementioned glands. Sicca symptoms are not obligatory but are common. Improvement is described after administration of corticosteroids. Sonographically, heterogeneous hypoechogenic lesions, and small cysts are described [56] [57].

Sialadenoses

Sialadenoses are characterized by chronic, non-inflammatory, non-neoplastic, usually bilateral hyperplasia, and metaplasia of the gland parenchyma. Clinically, a mostly painless persistent swelling of the salivary glands, especially the parotid glands, can be seen. Autoinflammatory or inflammatory diseases such as HIV or Sjögren’s syndrome are not included. From a pathophysiologic perspective, various aetiologies are suspected that end with a common autonomic nervous dysfunction [58]. This nervous dysfunction often occurs in the context of alcohol abuse or endocrine disorders. These include diabetes mellitus, pituitary and thyroid diseases, menopause, and adrenal cortex dysfunction. Malnutrition, especially anorexia nervosa or bulimia, as well as chronic kidney disease and the intake of certain medications such as antihypertensives or psychotropic drugs are also associated with this. However, in approximately 50 % of cases no aetiology can be diagnosed [58]. From a histological perspective, hypertrophy of the acinar cells with scattered fat cells is usually seen [59]. Sonographic examination reveals homogeneous hyperplasia of the salivary gland parenchyma, i. e. the salivary glands are enlarged, and the tissue is usually hyperechogenic.

 

MissingLinkText

 

MissingLinkText

 

MissingLinkText

Benign neoplasms

Ultrasound (US) is also the imaging modality of choice for tumors of the major salivary glands. If a tumor cannot be visualized completely using US, because it is too large, extends into the parapharyngeal space, or there are indications of malignancy, further cross-sectional imaging procedures should be considered.

Lymph nodes of the parotid gland are often not as well defined as those of the rest of the neck ([Fig. 11]). The entities of benign salivary gland tumors are diverse according to the WHO classification [60]. Overall, the most common benign salivary gland tumor is the pleomorphic adenoma (PA). In the parotid gland, PA and Warthin tumor (WT) both occur with equal frequency [61] [62] [63] [64]. WTs can occur multicentrically and bilaterally and are often oval in shape [65] [66] [67]. Preoperative differentiation of the different entities is preferable. This could make it possible to pursue various popular treatment concepts.

Fig. 11 Lymphadenopathy of the parotid gland

The shape and homogeneity may vary in all benign tumors. In the B-mode image, the benign tumors appear as smooth margins. However, in the context of inflammation or infarction of a WT, benign tumors may have blurred tumor boundaries. Benignomas of the salivary glands are often hypoechoic. In particular, WT have echo-free areas as an expression of the cystic parts [68] [69].

PAs may also show echo-free areas as an expression of necrosis. A lobulated aspect is more suggestive of PA ([Fig. 12]), but is not pathognomonic [68]. Distal acoustic events are more common in PA, but may also occur in WT depending on the cystic component [70]. Intratumoral calcifications are also occasionally described and may indicate PA.

Fig. 12 Pleomorphic adenoma of the parotid gland.

In color-coded duplex sonography (CCDS), many studies show significant differences in macrovascularization between PA and WT: While PAs are rather low or weakly vascularized, mostly peripherally ([Fig. 13]), WTs are rather strongly vascularized intratumorally and peripherally ([Fig. 14]) [68] [69] [71] [72]. They can show a tree-like branching. Depending on the size of the cystic portion, a rarification of vascularization can also be observed in WTs. Ultimately, many studies can describe characteristics for certain benign tumors in the B-mode image and in the CCDS scan, but due to large areas of overlap, it is not possible to clearly determine the entity.

Fig. 13 Pleomorphic adenoma of the parotid gland incl. Doppler examination.

Fig. 14 Warthin tumor of the parotid gland incl. Doppler examination.

In recent years, new procedures have been established in the US. Contrast-enhanced US (CEUS) provides good visualization of tumor perfusion, including microvascularization. Significant differences between the 2 entities have been observed in various perfusion parameters, although there is also some overlap depending on the composition of the tumor [71] [72]. Elastography showed that PAs are harder than WTs, but that histological heterogeneity in an entity has a strong influence on elastography. In particular, it is difficult to differentiate elastographically between PAs and malignancies [73] [74] [75].

Overall, the data on the new procedures are still too limited and somewhat contradictory to recommend these for routine examinations. One objective of many working groups is to incorporate a range of clinical and sonographic criteria in algorithms in order to optimize the sensitivity and specificity for entity or its dignity determination [74] [76]. A further challenge is the presence of additional benign tumors, which occur so rarely that it is difficult to make a statement about their characteristics.

 

MissingLinkText

Malignant neoplasms

Primary cancer of the major salivary glands represents a heterogeneous group of more than 20 different histological subtypes with considerable variations in cytopathological morphology. However, considerable overlap in histological, immunohistochemical, molecular profiles, and biological behaviour is observed [60].

In recent decades, the classifications of salivary gland malignancies have undergone regular changes in response to new molecular findings. These changes in the WHO classification, which are also “an evolving art” [77], reflect the evolution of our knowledge. Due to the gradient of histological complexity of these lesions, sonographic imaging also has its inherent limitations. The traditionally accepted sonographic B-mode pattern with poorly defined margins, inhomogeneity of echotexture, marked hypoechogenicity, as well as calcifications, suspected intraparotid or cervical lymph nodes, mostly occurs in advanced T categories or high-grade histological subtypes [78]. An overlap in ultrasound characteristics between benign tumors and initial T categories [79], as well as low-grade malignant subtypes, has been reported [80].

The vascularization pattern could potentially provide information about the physiobiological properties of the tumor [81]. In many malignant cases, a higher degree of vascularity ([Fig. 15]) with a scattered vascular pattern, higher velocities and higher vascular resistance is observed due to angiogenesis [82]. However, a predictive value has not yet been reliably established [79].

Fig. 15 Mucoepidermoid carcinoma of the parotid gland.

The highly variable architecture of salivary gland malignancies with different degrees of stiffness and the rigid chondromyxoid nature of pleomorphic adenomas make it difficult to reliably diagnose a malignant tumor via sonoelastography [83] [84]. In recent years, increased focus has been on the value of several sonoelastographic modalities (especially shear wave elastography) for predicting malignant salivary gland lesions. Faster shear waves and the distribution of higher shear wave velocities over larger tumor portions (higher tumor stiffness due to reactive interstitial fibrosis [83]) are associated with a higher risk of malignancy ([Fig. 16]) [85]. Shear wave elastography demonstrated pooled sensitivity rates of approximately 60 % [86].

Fig. 16 Squamous cell carcinoma of the left parotid gland: ARFI – shear wave elastography with shear velocity values of 10.0 m/s (red coloured intratumoral area reflecting high tissue stiffness), 7.36 m/s (red coloured intratumoral zone with yellow peripheral zone), 5.51 m/s (green coloured intratumoral area with cystic-necrotic differentiation), and 1.95 m/s (blue coloured area in the surrounding tissue of the tumor).

Contrast-enhanced ultrasound enables quantitative analysis of microvascular perfusion in solid parotid tumors. This can be combined with macrovascularization-related data from color-coded duplex sonography. This approach allows, for example, poor vascularization with increased perfusion kinetics or strong vascularization with delayed perfusion to be considered as signs of malignancy, although with moderate sensitivity [76].

Lymphoma manifestations of the salivary glands represent a complex sonographic entity that can easily simulate both benign and malignant diseases, sonographically [87]. Primary squamous cell carcinoma of the parotid gland, as well as lymph node metastases from squamous cell carcinoma, are described as heterogeneous, aggressive tumors that may also exhibit necrosis [67].

 

MissingLinkText

 

MissingLinkText

Conflict of Interest

Declaration of financial interests

Receipt of research funding: yes, from another institution (pharmaceutical or medical technology company, etc.) and a/the sponsor(s) of this training/educational unit; receipt of payment/financial advantage for providing services as a lecturer: yes, from another institution (pharmaceutical or medical technology company, etc.) and a/the sponsor(s) of this training/educational unit; paid consultant/internal trainer/salaried employee: yes, from another institution (pharmaceutical or medical technology company, etc.); patent/business interest/shares (author/partner, spouse, children) in company: none; patent/business interest/shares (author/partner, spouse, children) in sponsor of this CME article or in company whose interests are affected by the CME article: none.

Declaration of non-financial interests

The authors declare that they have no conflict of interest.

• References

• 1 Iro H, Zenk J. Speicheldrüsenerkrankungen im Kindesalter. Laryngorhinootologie 2014; 93: 103-125
• 2 Waldhausen JHT. Branchial cleft and arch anomalies in children. Semin Pediatr Surg 2006; 15: 64-69
• 3 Whitley MK, Zur KB. Salivary gland diseases in children. GMS Curr Top Otorhinolaryngol Head Neck Surg 2014; 13: 1467-1478
• 4 Friedman E, Patiño MO, Udayasankar UK. Imaging of Pediatric Salivary Glands. Neuroimaging Clin N Am 2018; 28: 209-226
• 5 Zhou Q, Zheng JW, Mai HM. et al. Treatment guidelines of lymphatic malformations of the head and neck. Oral Oncol 2011; 47: 1105-1109
• 6 Bradley P, McClelland L, Mehta D. Paediatric salivary gland epithelial neoplasms. ORL J Otorhinolaryngol Relat Spec 2007; 69: 137-145
• 7 Sultan I, Rodriguez-Galindo C, Al-Sharabati S. et al. Salivary gland carcinomas in children and adolescents: A population-based study, with comparison to adult cases. Head Neck 2011; 33: 1476-1481
• 8 Shapiro NL, Bhattacharyya N. Clinical characteristics and survival for major salivary gland malignancies in children. Otolaryngol Head Neck Surg 2006; 134: 631-634
• 9 Surun A, Schneider DT, Ferrari A. et al. Salivary gland carcinoma in children and adolescents: The EXPeRT/PARTNER diagnosis and treatment recommendations. Pediatr Blood Cancer 2021; 68: e29058
• 10 Yoshida EJ, García J, Eisele DW. et al. Salivary gland malignancies in children. Int J Pediatr Otorhinolaryngol 2014; 78: 174-178
• 11 McQuone SJ. Acute viral and bacterial infections of the salivary glands. Otolaryngol Clin North Am 1999; 32: 793-811
• 12 Hidalgo-Santos AD, Gastón-Téllez R, Ferrer-Lorente B. et al. Immune disorders associated with juvenile recurrent chronic parotitis. An Pediatr 2021; 95: 260-266
• 13 Francis CL, Larsen CG. Pediatric sialadenitis. Otolaryngol Clin North Am 2014; 47: 763-778
• 14 Ramakrishna J, Strychowsky J, Gupta M. et al. Sialendoscopy for the management of juvenile recurrent parotitis: A systematic review and meta-analysis. Laryngoscope 2015; 125: 1472-1479
• 15 Valour F, Sénéchal A, Dupieux C. et al. Actinomycosis: Etiology, clinical features, diagnosis, treatment, and management. Infect Drug Resist 2014; 7: 183-197
• 16 Kenechi NwawkaO, Nadgir R, Fujita A. et al. Granulomatous Disease in the Head and Neck: Developing a Differential Diagnosis. Radiographics 2014; 34: 1240-1257
• 17 Koch M, Sievert M, Iro H. et al. Ultrasound in Inflammatory and Obstructive Salivary Gland Diseases: Own Experiences and a Review of the Literature. J Clin Med 2021; 10
• 18 Mansour N, Bobenstetter L, Mansour S. et al. [Differentiation of ultrasonographic hypoechoic head and neck lesions]. Laryngorhinootologie 2019; 98: 701-707
• 19 Mantsopoulos K, Psychogios G, Agaimy A. et al. Inflamed benign tumors of the parotid gland: Diagnostic pitfalls from a potentially misleading entity. Head Neck 2015; 37: 23-29
• 20 Iro H, Zenk J, Koch M. [Modern concepts for the diagnosis and therapy of sialolithiasis]. HNO 2010; 58: 211-217
• 21 Zengel P, Schrötzlmair F, Schwarz F. et al. Elastography: A new diagnostic tool for evaluation of obstructive diseases of the salivary glands; primary results. Clin Hemorheol Microcirc 2012; 50: 91-99
• 22 Marchal F, Dulguerov P. Sialolithiasis management: The state of the art. Arch Otolaryngol Head Neck Surg 2003; 129: 951-956
• 23 Escudier MP, McGurk M. Symptomatic sialoadenitis and sialolithiasis in the English population, an estimate of the cost of hospital treatment. Br Dent J 1999; 186: 463-466
• 24 Williams MF. Sialolithiasis. Otolaryngol Clin North Am 1999; 32: 819-834
• 25 Kajander EO, Çiftçioglu N. Nanobacteria: An alternative mechanism for pathogenic intra- and extracellular calcification and stone formation. Proc Natl Acad Sci U S A 1998; 95: 8274-8279
• 26 Lustmann J, Regev E, Melamed Y. Sialolithiasis. A survey on 245 patients and a review of the literature. Int J Oral Maxillofac Surg 1990; 19: 135-138
• 27 Zengel P, Schrötzlmair F, Reichel C. et al. Sonography: The leading diagnostic tool for diseases of the salivary glands. Semin Ultrasound CT MR 2013; 34: 196-203
• 28 Mehanna H, McQueen A, Robinson M. et al. Salivary gland swellings. BMJ 2012; 345
• 29 Koch M, Iro H, Zenk J. [Stenosis and other non-sialolithiasis-related obstructions of the major salivary gland ducts. Modern treatment concepts]. HNO 2010; 58: 218-224
• 30 Kopeć T, Szyfter W, Wierzbicka M. et al. Stenoses of the salivary ducts-sialendoscopy based diagnosis and treatment. Br J Oral Maxillofac Surg 2013; 51
• 31 Koch M, Iro H, Zenk J. Role of sialoscopy in the treatment of Stensen’s duct strictures. Ann Otol Rhinol Laryngol 2008; 117: 271-278
• 32 Qi S, Liu X, Wang S. Sialoendoscopic and irrigation findings in chronic obstructive parotitis. Laryngoscope 2005; 115: 541-545
• 33 Rose SS. A Clinical and Radiological Survey of 192 Cases of Recurrent Swellings of the Salivary Glands: Hunterian Lecture delivered at the Royal College of Surgeons of England on 26th March 1953. Ann R Coll Surg Engl 1954; 15: 374
• 34 Zengel P, Berghaus A, Weiler C. et al. Intraductally applied contrast-enhanced ultrasound (IA-CEUS) for evaluating obstructive disease and secretory dysfunction of the salivary glands. Eur Radiol 2011; 21: 1339-1348
• 35 Vogl TJ, Al-Nawas B, Beutner D. et al. Updated S2K AWMF guideline for the diagnosis and follow-up of obstructive sialadenitis – Relevance for radiologic imaging. Rofo 2014; 186: 843-846
• 36 Witt RL, Iro H, Koch M. et al. Minimally invasive options for salivary calculi. Laryngoscope 2012; 122: 1306-1311
• 37 Harbison JM, Liess BD, Templer JW. et al. Chronic parotitis: A challenging disease entity. Ear Nose Throat J 2011; 90
• 38 Baurmash HD. Chronic recurrent parotitis: A closer look at its origin, diagnosis, and management. J Oral Maxillofac Surg 2004; 62: 1010-1018
• 39 Epivatianos A, Harrison JD. The presence of microcalculi in normal human submandibular and parotid salivary glands. Arch Oral Biol 1989; 34: 261-265
• 40 Brito-Zerón P, Theander E, Baldini C. et al. Early diagnosis of primary Sjögren’s syndrome: EULAR-SS task force clinical recommendations. Expert Rev Clin Immunol 2016; 12: 137-156
• 41 Psianou K, Panagoulias I, Papanastasiou AD. et al. Clinical and immunological parameters of Sjögren’s syndrome. Autoimmun Rev 2018; 17: 1053-1064
• 42 Milic VD, Petrovic RR, Boricic IV. et al. Diagnostic value of salivary gland ultrasonographic scoring system in primary Sjogren’s syndrome: A comparison with scintigraphy and biopsy. J Rheumatol 2009; 36: 1495-1500
• 43 Mossel E, Delli K, Van Nimwegen JF. et al. Ultrasonography of major salivary glands compared with parotid and labial gland biopsy and classification criteria in patients with clinically suspected primary Sjögren’s syndrome. Ann Rheum Dis 2017; 76: 1883-1889
• 44 Hočevar A, Ambrožič A, Rozman B. et al. Ultrasonographic changes of major salivary glands in primary Sjogren’s syndrome. Diagnostic value of a novel scoring system. Rheumatology (Oxford) 2005; 44: 768-772
• 45 Lin D, Yang W, Guo X. et al. Cross-sectional comparison of ultrasonography scoring systems for primary Sjogren’s syndrome. Int J Clin Exp Med 2015; 8: 19065
• 46 Mossel E, Arends S, Van Nimwegen JF. et al. Scoring hypoechogenic areas in one parotid and one submandibular gland increases feasibility of ultrasound in primary Sjögren’s syndrome. Ann Rheum Dis 2018; 77: 556-562
• 47 Cornec D, Jousse-Joulin S, Marhadour T. et al. Salivary gland ultrasonography improves the diagnostic performance of the 2012 American College of Rheumatology classification criteria for Sjögren’s syndrome. Rheumatology (Oxford) 2014; 53: 1604-1607
• 48 Le GoffM, Cornec D, Jousse-Joulin S. et al. Comparison of 2002 AECG and 2016 ACR/EULAR classification criteria and added value of salivary gland ultrasonography in a patient cohort with suspected primary Sjögren’s syndrome. Arthritis Res Ther 2017; 19
• 49 Hofauer BG. Etablierung sonographischer Marker zur Diagnose und Verlaufskontrolle des primären Sjögren-Syndroms.
• 50 Knopf A, Hofauer B, Thürmel K. et al. Diagnostic utility of Acoustic Radiation Force Impulse (ARFI) imaging in primary Sjoegren’s syndrome. Eur Radiol 2015; 25: 3027-3034
• 51 Nikolopoulos D, Kitsos D, Papathanasiou M. et al. POS0123 Major salivary gland ultrasonography and MRI with diffusion weighted imaging (DWI) as complementary tools to identify features of malt in primary Sjögren’s Syndrome (PSS): A single center cross sectional study. Ann Rheum Dis 2022; 81: 287-287
• 52 Ko KWS, Bhatia KS, Ai QYH. et al. Imaging of head and neck mucosa-associated lymphoid tissue lymphoma (MALToma). Cancer Imaging 2021; 21: 1-8
• 53 Knopf A, Lahmer T, Chaker A. et al. Head and neck sarcoidosis, from wait and see to tumor necrosis factor alpha therapy: A pilot study. Head Neck 2013; 35: 715-719
• 54 Hofauer B, Wiesner M, Stock K. et al. Multimodal Evaluation of Long-Term Salivary Gland Alterations in Sarcoidosis. J Clin Med 2022; 11: 2292
• 55 Puxeddu I, Capecchi R, Carta F. et al. Salivary Gland Pathology in IgG4-Related Disease: A Comprehensive Review. J Immunol Res 2018;
• 56 Narayan AK, Baer A, Fradin J. Sonographic findings of IgG4-related disease of the salivary glands: Case report and review of the literature. J Clin Ultrasound 2018; 46: 73-77
• 57 Moore AE, Marcus KS, Rajan KD A. et al. Ultrasound and Sialogram Correlates to Parotid Immunoglobulin G4-Related Disease. Ear Nose Throat J 2021; 103: 247-251
• 58 Davis AB, Hoffman HT. Management Options for Sialadenosis. Otolaryngol Clin North Am 2021; 54: 605-611
• 59 Scully C, Bagán JV, Eveson JW. et al. Sialosis: 35 cases of persistent parotid swelling from two countries. Br J Oral Maxillofac Surg 2008; 46: 468-472
• 60 Skálová A, Hyrcza MD, Leivo I. Update from the 5^th Edition of the World Health Organization Classification of Head and Neck Tumors: Salivary Glands. Head Neck Pathol 2022; 16: 40-53
• 61 Psychogios G, Vlastos I, Thölken R. et al. Warthin’s tumour seems to be the most common benign neoplasm of the parotid gland in Germany. Eur Arch Oto-Rhino-Laryngology 2020; 277: 2081-2084
• 62 Piwowarczyk K, Bartkowiak E, Klimza H. et al. Review and characteristics of 585 salivary gland neoplasms from a tertiary hospital registered in the Polish National Major Salivary Gland Benign Tumors Registry over a period of 5 years: A prospective study. Otolaryngol Pol = Polish Otolaryngol 2020; 74: 1-6
• 63 Kato H, Kawaguchi M, Ando T. et al. Pleomorphic adenoma of salivary glands: common and uncommon CT and MR imaging features. Jpn J Radiol 2018; 36: 463-471
• 64 Mantsopoulos K, Iro H. Pleomorphic adenoma compared with cystadenolymphoma of the parotid gland: Which is more common?. Br J Oral Maxillofac Surg 2020; 58: 361-363
• 65 Franzen AM, Kaup FranzenC, Guenzel T. et al. Increased incidence of Warthin tumours of the parotid gland: A 42-year evaluation. Eur Arch Oto-Rhino-Laryngology 2018; 275: 2593-2598
• 66 Patel DK, Morton RP. Demographics of benign parotid tumours: Warthin’s tumour versus other benign salivary tumours. Acta Otolaryngol 2016; 136: 83-86
• 67 Gritzmann Radiologie Und Nuklearmedizin N, Der Barmherzigen Brüder K, Schlüsselwörter S, et al. Ultraschall der Speicheldrüsen Ultrasound of the Salivary Glands. Otol 2009; 88: 48-59
• 68 Rong X, Zhu Q, Ji H. et al. Differentiation of pleomorphic adenoma and Warthin’s tumor of the parotid gland: Ultrasonographic features. Acta Radiol 2014; 55: 1203-1209
• 69 Matsuda E, Fukuhara T, Donishi R. et al. Usefulness of a Novel Ultrasonographic Classification Based on Anechoic Area Patterns for Differentiating Warthin Tumors from Pleomorphic Adenomas of the Parotid Gland. Yonago Acta Med 2017; 60: 220
• 70 Mansour N, Stock KF, Chaker A. et al. Evaluation of parotid gland lesions with standard ultrasound, color duplex sonography, sonoelastography, and acoustic radiation force impulse imaging – a pilot study. Ultraschall in Med 2012; 33: 283-288
• 71 Mansour N, Bas M, Stock KF. et al. Multimodal Ultrasonographic Pathway of Parotid Gland Lesions. Ultraschall in Med 2017; 38: 166-173
• 72 Yan M, Xu D, Chen L. et al. Comparative Study of Qualitative and Quantitative Analyses of Contrast-Enhanced Ultrasound and the Diagnostic Value of B-Mode and Color Doppler for Common Benign Tumors in the Parotid Gland. Front Oncol 2021; 11
• 73 Matsuda E, Fukuhara T, Donishi R. et al. Clinical Utility of Qualitative Elastography Using Acoustic Radiation Force Impulse for Differentiating Benign from Malignant Salivary Gland Tumors. Ultrasound Med Biol 2021; 47: 279-287
• 74 Guiban O, Rubini A, Fresilli D. et al. Preoperative Multiparametric Ultrasound and Fine Needle Aspiration Cytology evaluation of parotid gland tumors: Which is the best technique?. Med Ultrason 2021; 23: 402-409
• 75 Olgun DC, Kantarci F, Taskin U. et al. Relative proportions of stromal to cellular components of pleomorphic adenomas: Determination with shear wave elastography. J Ultrasound Med 2014; 33: 503-508
• 76 Mansour N, Bas M, Stock KF. et al. Multimodal Ultrasonographic Pathway of Parotid Gland Lesions. Ultraschall in Medizin 2017; 38: 166-173
• 77 Mantsopoulos K, Mueller S, Goncalves M. et al. Completion surgery after extracapsular dissection of low-grade parotid gland malignant tumors. Head Neck 2019; 41: 3383-3388
• 78 Martino M, Fodor D, Fresilli D. et al. Narrative review of multiparametric ultrasound in parotid gland evaluation. Gland Surg 2020; 9: 2295-2311
• 79 Bozzato A, Zenk J, Greess H. et al. Potential of ultrasound diagnosis for parotid tumors: Analysis of qualitative and quantitative parameters. Otolaryngol Head Neck Surg 2007; 137: 642-646
• 80 Berner F, Koch M, Müller SK. et al. Investigation of Sonographic Criteria for Reliable Identification of T1-T2 Low-Grade Malignant Tumors of the Parotid Gland. Ultrasound Med Biol 2021; 47: 471-477
• 81 Knopf A, Mansour N, Chaker A. et al. Multimodal ultrasonographic characterisation of parotid gland lesions – a pilot study. Eur J Radiol 2012; 81: 3300-3305
• 82 El-Khateeb SM, Abou-Khalaf AE, Farid MM. et al. A prospective study of three diagnostic sonographic methods in differentiation between benign and malignant salivary gland tumours. Dentomaxillofacial Radiol 2011; 40: 476
• 83 Heřman J, Sedláčková Z, Vachutka J. et al. Differential Diagnosis of Parotid Gland Tumors: Role of Shear Wave Elastography. Biomed Res Int 2017;
• 84 Thimsen V, Goncalves M, Koch M. et al. The current value of quantitative shear wave sonoelastography in parotid gland tumors. Gland Surg 2021; 10: 1374-1374
• 85 Jering M, Zenk J, Thölken R. et al. Can Ultrasound in Combination with Virtual Touch Imaging Quantification Predict the Dignity of a Parotid Tumor?. Ultrasound Med Biol 2021; 47: 1192-1203
• 86 Zhang YF, Li H, Wang XM. et al. Sonoelastography for differential diagnosis between malignant and benign parotid lesions: A meta-analysis. Eur Radiol 2019; 29: 725-735
• 87 Mantsopoulos K, Koch M, Fauck V. et al. Primary parotid gland lymphoma: Pitfalls in the use of ultrasound imaging by a great pretender. Int J Oral Maxillofac Surg 2021; 50: 573-578

Publication History

Received: 27 February 2024

Accepted after revision: 14 November 2024

Article published online:
17 January 2025