Bilateral submandibular gland nodular oncocytic hyperplasia with papillary cystadenoma-like areas

Abstract

A 57-year-old man presented in 2016 with a 4-month history of a right submandibular mass, having undergone left submandibular gland (SMG) excision in 2003. Imaging suggested a benign tumour and subsequent core biopsy findings suggested a nodular oncocytic hyperplasia, similar to the tumour removed from the contralateral side. This was confirmed on histological analysis following right submandibular gland excision which showed characteristic features of nodular oncocytic hyperplasia along with an unusual diffuse papillary cystadenoma-like ductal proliferation, similar to that seen in the 2003 specimen. A diagnosis of multinodular adenomatous oncocytic hyperplasia (MAOH) was rendered in order to communicate the unique histological features that have otherwise not been described in the literature. We believe that this is the first reported case of non-synchronous multinodular oncocytic hyperplasia and the first case affecting the submandibular glands.

Background

Nodular oncocytic hyperplasia (NOH) is a rare, benign condition characterised by presence of multiple nodules on oncocytic cells within one or both parotid glands.¹ Accordingly, it has previously only been reported as developing within the parotid gland, either in isolation or presenting in a synchronous manner. This case provides a new insight into this lesion, suggesting that it can manifest in any major salivary tissue, it has the potential to develop de novo in multiple glands and that it may be associated with a papillary cystadenoma-like ductal proliferation on histology. It also emphasises the importance of both multimodal imaging of neck masses and closed biopsy as well as correlating current histopathological results with previous reports.

Case presentation

A 57-year-old man presented to our ear, nose and throat service in August 2016 with a 4-month history of a mass in the right submandibular region. It had slowly been increasing in size during this period but was not associated with any pain or other local/systemic complications. The patient’s medical history included pulmonary embolism in 2013, gastro-oesophageal reflux disease and having undergone a left submandibular gland excision in 2003. He used no medication and reported no drug allergies. He was a non-smoker and non-drinker and worked as an office manager.

On examination, a non-tender 2.5 cm mass was identified in the right level I area that was firm in consistency and taking apparent origin from deep tissue structures, rather than the skin. There was no associated cervical lymphadenopathy, and examination of the skin, oral cavity, oropharynx and flexible nasolaryngoscopy was normal.

Investigations

Ultrasound imaging suggested that the mass had an atypical appearance with features principally in keeping with chronic sialadenitis, including atrophy, hypoechogenicity and irregular margins. These features were unchanged 2 months later on repeat ultrasonography. Ultrasound-guided core biopsy suggested the mass was an NOH on histopathological analysis (figure 1). The core biopsy diagnosis was aided by comparing with the excised left submandibular gland (SMG) pathology slides from 14 years earlier (figure 2). MRI with contrast identified that the whole of the right SMG had been consumed by infiltration of the lesion but with no extension beyond the capsule of the gland itself (figure 3) and no involvement of the parotid glands. In retrospect, it was felt that both the ultrasound imaging and the MRI scan added little to narrow the differential diagnoses before histological examination, but debate remains around their merit in the investigation of such cases.

Figure 1.

Histology of right submandibular gland lesion at x20 magnification, stained using H&E. Black stars, zones of oncocytic change; black arrows, dilated cystadenoma-like areas; blue stars, normal background SMG.

Figure 2.

Histology of left submandibular gland lesion, 13 years previously (2003) at x20 magnification, stained using H&E. Black stars, zones of oncocytic change; black arrows, dilated cystadenoma-like areas; blue stars, normal background SMG.

Figure 3.

MRI scan showing right submandibular gland infiltrated with MAOH (note previously excised left submandibular gland). MAOH, multinodular adenomatous oncocytic hyperplasia.

Differential diagnosis

The differential diagnosis in this case included:

• Submandibular sialadenitis.

• Submandibular sialectasis.

• Submandibular lymphoma.

• Benign submandibular tumour, in particular a pleomorphic salivary adenoma.

• Submandibular gland malignancy such as Warthin’s tumour, oncocytoma or oncocytic carcinoma (these are particularly important to consider, as many of these lesions can include oncocytes).

Treatment

Following discussion of the case with radiological and histopathological review at our regional head and neck cancer multidisciplinary team meeting, a decision was made to excise the whole submandibular gland to gain a definitive histology diagnosis and to guide any further management. The right SMG excision proceeded well with no perioperative or postoperative complications. Histopathological analysis of the whole gland confirmed the diagnosis made from the original core biopsy sample and that the lesion had been fully excised, with the capsule intact.

Outcome and follow-up

Following postoperative review 1 month after surgery, the patient was discharged from the care of our service with no plans for follow-up.

Discussion

The nature of masses within the submandibular gland and area is varied and may carry a wide differential diagnosis. The presentation only broadly correlates with patients’ clinical history and examination, and so radiological imaging with or without fine-needle aspiration cytology or core biopsy remains the important investigation in reaching a diagnosis. Open biopsy is to be avoided unless previous investigations remain inconclusive.² Ultrasonography remains a useful initial radiological investigation due to relative ease of access compared with CT and MRI and greater sensitivity and specificity than plain X-ray. Ultrasound imaging also allows needle and trephine biopsies to be far better guided than by free hand, improving accuracy. MRI remains the best method of imaging soft tissue within the head and neck region, allowing better distinction between tissue planes and fat suppression to distinguish between solid and non-solid pathology. This case can provide a useful example of how a stepwise approach to the neck mass provides a safe and accurate diagnosis leading to appropriate treatment.

NOH is a rare, benign salivary tumour-like lesion described as occurring exclusively in the parotid gland.¹ To our knowledge, only eight cases have been reported previously since it was originally identified in 1986.^3–9 It overwhelmingly develops in females (M:F ratio is 1:7) and most commonly manifests in the sixth decade of life. All cases prior to this developed in the parotid gland, one possible explanation being due to the larger volume of tissue compared with the other major and minor salivary glands. Only a single case has been reported where bilateral, simultaneous development occurred.⁹ While a familial association was originally postulated, this has not been consistently demonstrated.³ Surgical excision has always been described as the principal treatment to definitively manage the tumour and to gain a diagnosis, and no further treatment after surgery has ever been required.

While both of the lesions reported here showed classic features of NOH, the finding of widespread papillary cystadenoma-like ductal proliferations between nodules is considered histologically unique.

Learning points.

• Submandibular masses have a wide differential diagnosis, with aetiology broadly correlating with clinical history and examination.

• Nodular oncocytic hyperplasia can develop out-with the parotid gland and may represent a field of histological change within the salivary tissues.

• Clinical examination combined with non-open biopsy and multimodal imaging remains a reliable and repeatable method for the assessment of neck masses.

• While the long-term cellular behaviour and prognosis of multinodular adenomatous oncocytic hyperplasia (MAOH) remains unknown, full surgical excision is advised to gain definite histological definition.

• Nodular oncocytic hyperplasia may show oncocytic papillary cystadenoma-like areas on histology.