Salivary gland neoplasms encompass a wide array of different histologies and locations, including the parotid, submandibular gland, sublingual gland, and minor salivary glands of the upper aerodigestive tract. The majority (80%) of these neoplasms are benign but are heterogeneous in their ability to recur and/or transform into malignant lesions. Therefore, correct diagnosis is essential in dictating the proper treatment. The World Health Organization (WHO) in 2017 recognized 11 different benign epithelial salivary gland tumors.
The most common benign subtypes identified include pleomorphic adenoma (PA), Warthin’s tumor (WT), and myoepithelioma (MYO), followed by rarer histologies including lymphadenoma (LA), sebaceous adenoma (SA), oncocytoma (OC), cystadenoma, sialadenoma papilliferum (SP), ductal papilloma (intraductal and inverted), canalicular adenoma (CA), and basal cell adenoma (BCA).
The etiology of benign salivary tumors is unknown but has been linked to radiation, smoking, trauma, viruses, and genetics. Studies have shown a correlation between salivary gland tumors and prior radiation exposure with 50% of radiation-induced tumors being pleomorphic adenoma. Although exposure to tobacco and alcohol is not associated with an increased risk of some salivary tumors, studies have reported a strong association between Warthin’s tumor and tobacco smoking. Increased IgG4-positive plasma cells in lymphadenoma suggest a role for immunomodulation in its development.
Ductal papilloma (intraductal type) is suspected to occur secondary to oral trauma and is usually found at the lower lip, floor of mouth, palate, and tongue. Ductal papilloma (inverted type) has been associated with Human Papillomavirus (HPV) types 6 and 11, as well as oral trauma. A chromosomal translocation involving 8q12 and rearrangement at 12q13-15 activates the pleomorphic adenoma gene 1 (PLGA1) and high-mobility group AT-hook 2 (HMGA2), respectively. PLGA1 and HMGA2 are highly specific for pleomorphic adenomas and carcinoma ex-pleomorphic adenomas.
Salivary gland neoplasms most commonly affect women with an overall male to female ratio of 1 to 1.5 and a male to female ratio of 1:1.6 for benign tumors. Children account for less than 5% of all salivary gland tumor cases, with the majority of the histology favoring benign and vascular tumors.
The parotid gland is the most common location for salivary gland tumors, comprising 60-75% of all cases. Around 85% of parotid tumors reside in the superficial lobe, 11% in the deep lobe, and 1% in the accessory lobe. The most common benign neoplasms found in the parotid are pleomorphic adenoma (53.3%-85%), Warthin's tumor (25%-32%), Basal cell adenoma (2% to 7%), Myoepithelioma (1% to 3%), Oncocytoma (1%).
The submandibular gland encompasses 10 to 15% of all salivary gland tumors with an even distribution of benign and malignant neoplasms. The most common benign submandibular tumor is a pleomorphic adenoma, which consists of 36% of all submandibular tumors.
Sublingual gland tumors are extremely rare. The most common benign sublingual gland tumor is pleomorphic adenoma.
Minor salivary glands comprise 9.5% to 14.7% of all salivary gland tumors, with the most commonly affected site being the palate.There is an equal distribution between benign and malignant tumors. The most common benign minor salivary gland tumors are pleomorphic adenoma, cystadenoma, and canalicular adenoma.
In a series of 216 benign salivary tumors, 138 (64%) were pleomorphic adenomas (PA), followed by Warthin's tumor (23%), recurrent pleomorphic adenoma (5.1%), oncocytoma (2.8%), myoepithelioma (1.9%), cystadenoma (1.4%) and basal cell adenoma (0.9%).
Salivary gland tumors are heterogeneous in their morphology and are postulated to develop from the same stem-cell differentiation pathways as normal salivary gland tissues. Four main theories have been proposed. These include the basal reserve cell theory, pluripotent unicellular reserve cell theory, semi-pluripotent bicellular reserve cell theory, and the multicellular theory.
Pleomorphic adenoma consists of varying amounts of epithelial and mesenchymal components. The epithelial elements give rise to ducts, whereas the mesenchymal elements give rise to cartilaginous, osseous, hyaline, and myxoid tissues. The mesenchymal component develops from a metaplastic process of the myoepithelial cells. Pleomorphic adenomas of the major salivary glands are encapsulated, whereas those from minor salivary glands are not. Pleomorphic adenoma often has an irregular border with finger-like projections (pseudopodia) that grow into the surrounding tissue making local recurrence a frequent occurrence if these tumors are not completely excised. In metastasizing pleomorphic adenoma (MPA), the histology resembles the original pleomorphic adenoma with occasional mitotic figures and pleomorphism but is not overtly histologically malignant.
Warthin tumor presents with a classic bi-layered eosinophilic, oncocytic epithelium with papillary projections and interspersed goblet cells. The epithelium is surrounded by a stroma of varying amounts of lymphoid tissue and germinal centers. The lymphocytic component, poor blood supply, and cystic spaces surrounding oncocytic cells make Warthin's tumor especially suspective to infarction, parotitis, and a 10x higher risk of inflammation following invasive procedures.
Myoepitheliomas are well-circumscribed, encapsulated masses of myoepithelial cells with spindle, epithelial, plasmacytoid, and clear cytoplasmic features. The cells are surrounded by mucoid, collagenous, or vascular stroma. The absence or minimal presence of ductal structures distinguishes myoepithelioma from pleomorphic adenoma.
Lymphadenoma is a well-circumscribed, encapsulated tumor of epithelial and lymphoid components. The non-sebaceous lymphadenoma variant contains epithelial (squamous or basaloid) cells surrounded by an intense lymphoid stroma. The sebaceous variant is more common (60%) and has epithelial cells with sebaceous differentiation. Lymphadenoma can be misdiagnosed as metastatic adenocarcinoma or lymphoepithelial carcinoma.
Sebaceous adenoma is a well-circumscribed, encapsulated mass with solid nests of sebaceous cells in a fibrous stroma. Occasional oncocytic metaplasia and foreign body giant cells can be present.
Oncocytoma is a well-circumscribed tumor with large epithelial, oncocytic cells with granulated eosinophilic cytoplasm surrounded by fibrovascular stroma nests, sheets, trabeculae, or ductal structures.
Cystadenoma is a well-circumscribed, non-encapsulated, multi-cystic mass. It contains a proliferative, papillary, and oncocytic epithelium and with papillary projections into the lumen. The lumen is filled with inflammatory, squamous, and foamy cells. There is no cellular atypia, mitotic figures, or invasive growth.
Sialadenoma papilliferum is a non-encapsulated, biphasic tumor consisting of an exophytic, hyperplastic squamous epithelium overlying deeper ductal elements (often creating cleft-like cystic spaces where both cell types are fused) in a papillary growth pattern. These tumors most commonly (>80%) occur in the oral cavity. Essentially, the salivary ductal cells expand in a biphasic growth pattern into the surrounding squamous keratotic epithelium and can cause hyperplasia and papillomatosis.
Ductal papilloma (intraductal type) consists of a papillary network of vascular fronds lined with the same columnar-cuboidal cells found on dilated salivary ducts. The papilla is often filling part of the cystic cavity. Cellular atypia and mitosis are usually absent.
Ductal papilloma (inverted type) presents with epithelial cells that form a broad papillary projection. Columnar cells, mucous cells, and microcysts can be present. There are few mitotic figures, and it is similar in histology to sinonasal inverted papilloma.
Canalicular adenoma consists of a bi-layered strand formed by columnar and cuboidal cells with eosinophilic cytoplasm. A vascular stroma separates the strands. squamous balls (morules), microliths, and tyrosine crystals may be present.
Basal cell adenoma is an encapsulated mass comprised of uniform basaloid epithelial cells and inner ductal epithelial cells with 4 distinct growth patterns: solid, trabecular, tubular, and membranous. The solid type is similar to the skin's basal cell carcinoma with solid nests of basaloid cells surrounded by an outer layer of columnar/cuboidal cells. The trabecular type has basaloid cells arranged in narrow strands and cords separated by a fibrous and vascular stroma. The tubular type has basaloid cells and multiple small duct lumens lined by eosinophilic, cuboidal cells. A combination of a tubule-trabecular pattern is often present and more common than the solid type. The membranous type differs from the other 3 patterns in that it is unencapsulated with multiple nests of basaloid cells, palisading peripheral cells, and thick hyaline material surrounding the epithelial islands. It can be multinodular with an invasive growth pattern.
Patients with salivary gland tumors often present with a long-standing history of a painless, palpable mass. A detailed history, including pain symptoms, the onset of the mass, growth rate, swallowing difficulties, and facial weakness symptoms, should be obtained. Past medical history, surgical history, family history of malignancies, and social risk factors (such as smoking, past radiation exposure, and occupational hazards) should be elicited.
Physical exam should include a focused head and neck exam. Both benign and malignant tumors can present as painless, fixed masses. Parotid masses most commonly occur at the superficial lobe. Deep parotid lobe tumors are often asymptomatic but can present with oropharyngeal airway narrowing, sleep apnea, or dyspnea on exertion. Submandibular tumors present with overall glandular enlargement, and sublingual tumors present with diffuse swelling at the mouth floor. Bimanual palpation of salivary masses can help elicit the tumor size and mobility.
The evaluation may include:
Ultrasound: Ultrasound is the initial non-invasive modality for localizing superficial tumors; distinguishing solid masses from cystic collections, and helping guide fine-needle aspiration biopsy.
Computerized tomography (CT): Conventional CT and MRI have similar sensitivity and specificity in determining tumor location, tumor margin, and tumor infiltration. Although CT has a lower resolution than MRI for soft tissue, CT provides an advantage in detecting early cortical bony invasion of the mandible.
Magnetic resonance imaging (MRI): For lesions in the deep parotid lobe, sublingual glands, and minor salivary glands, MRI provides an accurate extent of the tumor, the location of the tumor, and its relationship to the facial nerve, for preoperative planning purposes. MRI can quantify the diffusion properties of water in tumor tissue into the apparent diffusion coefficient (ADC). Diffusion-weighted MRI is useful for PA due to its higher ADC. Salivary gland malignancies have significantly smaller ADC than benign tumors, although the ADC of Warthin’s tumor is even smaller than that of malignancies due to excessive lymphoid tissue resembling lymphoma.
Positron emission tomography (PET). Compared with conventional CT, PET may be more accurate in demonstrating tumor extension, nodal involvement, local recurrence, and distant metastasis due to the tissues’ higher levels of standardized uptake values (SUV). However, PET is unable to differentiate between benign and malignant tumors due to pleomorphic adenoma and Warthin’s tumor both exhibiting high glucose uptake values.
Biopsy. Imaging is unable to completely distinguish between benign and malignant lesions. Obtaining histological samples is key to determining treatment options. Fine needle aspiration (FNA) is a safe diagnostic tool with a high level of accuracy including sensitivity and specificity of 73% and 91%, respectively, in distinguishing benign from malignant tumors. However, FNA may sometimes falter in its ability to determine the specific malignant subtype and tumor grade. Ultrasound-guided core needle biopsy (CNB) is able to obtain larger tissue specimens with histologic architecture which improves recognition of tumor grading and subtyping. However, disadvantages of CNB include more pain, need for local anesthesia, and increased risk of facial nerve injury and hematoma. The intraoperative frozen section has a sensitivity and specificity of 90% and 99%, respectively in distinguishing between benign and malignant lesions.
The mainstay of treatment for benign salivary lesions is complete surgical excision with negative margins. Radiation and medical therapy play little role in the treatment of benign salivary tumors. However, radiation has been utilized in cases of recurrent disease, extensive facial nerve involvement, and non-surgical candidates to improve local control. Repeated surgical interventions increase the risk of tumor spillage and facial nerve damage.
Surgical excision is the treatment of choice for benign salivary tumors. Enucleation is not advised due to the higher rates of local recurrence.
Lesions of the superficial lobe of the parotid gland can be excised with a superficial parotidectomy. Total parotidectomy with facial nerve preservation is performed for large superficial tumors, deep parotid tumors, or cases of metastasizing pleomorphic adenoma. Superficial parotidectomy involves elevating the skin flap over the parotid capsule, identifying the facial nerve trunk, and dissecting along all its branches, preserving the facial nerve if uninvolved by malignancy, and removal of the superficial lobe of the parotid containing the tumor while maintaining the integrity of the tumor pseudocapsule.
The disadvantages of superficial parotidectomy include excessive resection of parotid tissue leading to loss of parotid function, disruption of Stenson’s duct, facial contour defects, and facial nerve paralysis. Gland-preserving surgery has been recommended for benign tumors with a reduction in surgical complications and improvement in patient quality of life. An alternative procedure, the partial superficial parotidectomy, has been proposed where the tumor is resected with a normal margin of parotid tissue, and the facial nerve is only dissected in the vicinity of the tumor. A comparison of the two techniques was studied by Roh et al who found better cosmesis, sensory, and salivary functions along with less facial nerve weakness and no difference in recurrence rate for partial superficial parotidectomy.
Extracapsular dissection (ECD) is the most conservative approach and involves removing the tumor with only the immediate pseudocapsule without identifying nor dissecting the facial nerve branches. George et al showed that complications such as facial nerve damage, sialocele, and Frey syndrome were rare during ECD. In studies comparing ECD with superficial parotidectomy for benign tumors, superficial parotidectomy showed a higher rate of facial nerve complications.
Extirpation of the entire submandibular gland is the treatment of choice for benign submandibular tumors. However, this can lead to decreased resting salivary production. Studies that evaluated grand-preserving partial sialadenectomy for benign submandibular tumors showed that patients had higher postoperative resting saliva rates and less facial deformity with no difference in local control. Gland preservation surgery is contraindicated for malignant tumors and central gland lesions that would risk damage to the vascular and ductal integrity of the remaining salivary tissue after partial sialoadenectomy.
For benign minor salivary gland tumors of the palate, a wide local excision within the palatal mucosa is recommended with 5 to 10 mm margins and preservation of the pseudocapsule. The exposed palatine bone is left to heal by secondary intention or resected and reconstructed with soft tissue flap.
Surgical resection with negative margins achieves local control in over 95% of benign salivary gland tumor cases. Postoperative radiation is usually not recommended in these cases due to the small benefit in local control and potential risk for radiation morbidity. However, in cases of incomplete tumor resection or spillage, adjuvant RT was found to significantly reduce the rate of local recurrence and reduce the risk of facial nerve injury from reoperation.
Recurrent PA can be seen in 0% to 23% of cases, and a second surgery is recommended for local control. In cases of multinodular recurrence or metastasizing pleomorphic adenoma, adjuvant radiation has been shown to achieve improved local control. Postoperative radiation has also been proposed to treat PA where surgery is unlikely to clear the disease, where there is facial nerve involvement, history of multiple recurrences, and in elderly patients who are poor surgical candidates.
The prognosis of benign salivary gland tumors varies widely based on the myriad of tumor histologies with different rates of recurrence and malignant transformation.
Surgical excision is the standard of treatment for all salivary gland tumors. This may lead to a loss of functional tissue and saliva secretion, causing xerostomia, dental caries, halitosis, periodontal disease, and oral infections. The incidence of temporary facial nerve palsy after parotidectomy ranges from 10% to 65%, with permanent paralysis seen in less than 5%. The incidence of Frey syndrome after parotidectomy varies widely from 2% to 80% due to the time interval since surgery as well as the surveillance criteria from the surgeons.
Treatments for Frey syndrome have included antiperspirant ointment, botulinum toxin A injections, and barrier flaps such as superficial musculoaponeurotic system (SMAS) flap, temporoparietal flap, sternocleidomastoid flap, anterolateral thigh flap, or thick skin flap. Additional complications from surgical resection include sialocele, salivary fistula, neuromas of the great auricular nerve, and preauricular skin anesthesia.
Complications from radiation include sensorineural hearing loss, chronic otitis media/externa, otalgia, skin erythema, mucositis, dysphagia, dysgeusia, xerostomia, soft tissue fibrosis, osteoradionecrosis, and radiation-induced malignancy. Approximately 36% of patients were found to develop hearing loss of 10 dB and higher at 4kHz. Mandibular osteoradionecrosis (<2%) and RT-induced malignancy (1%) at 10 to 25 years are rare complications.
Diagnosis and management of salivary malignancies would need to consist of an interprofessional team, including an otolaryngologist, plastic surgeon, general surgeon, radiation oncologist, speech-language pathologist, and primary care physician.
Patient education on salivary tumors can be challenging due to the heterogeneous array of histologies and the need for multidisciplinary and multimodal management. Patients and their families should be educated on the different treatment options and timeline, including surgical resection, radiation therapy if indicated, and long-term follow-up for recurrence. Patients and parents should be counseled on the possible risks and complications of all treatment modalities and their comorbidities fully assessed by their primary care physicians to determine if they will be candidates for surgical resection. Long-term follow-up is crucial for benign salivary tumors and must be emphasized to patients, given the risk of recurrence and malignant transformation of certain histologies.
Patients with benign salivary gland tumors should be managed by a multidisciplinary team of otolaryngologists, plastic surgeons, general surgeons, pathologists, radiation oncologists, speech-language pathologists, and primary care physicians. Salivary tumors present with varying histologies and severities requiring therapy involving surgery and occasional radiation for recurrent or invasive diseases. Close communication and collaboration between the surgeons and radiation oncologists can provide a tailored approach for each patient. Difficulties with swallowing can occur from acute radiation toxicity.
Patients may need a consultation with general surgery for gastric tube placement to ensure optimal nutrition through treatment, especially if radiation therapy is planned. Early post-treatment intervention by speech-language pathologists can help patients regain pre-treatment function to prevent malnutrition and dependence on enteric feeding. Facial nerve paralysis may occur after parotid surgery, and consultation with an otolaryngologist or plastic surgeon for facial nerve rehabilitation is recommended.
Recurrence of salivary tumors can occur after incomplete excision, and malignant transformation can occur several years after initial treatment. Thus, routine close follow-up by the otolaryngologist, radiation oncologists, and primary care physician is advocated. Finally, patients may develop depression, social anxiety, and avoidance due to visible surgical scarring and facial nerve paralysis. Formal peer support groups can aid patients in addressing their concerns.
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