Oncocytic Lipoadenoma: Report of 3 Rare Cases Involving the Parotid Gland,Including a Synchronous Presentation With Paraganglioma of the Right Carotid Bifurcation and Literature Review

Abstract

Oncocytic lipoadenoma (OL) is a rare salivary gland tumor characterized by the presence of oncocytic cells and mature adipose tissue. To date, only 30 cases of OL have been reported in the English-language literature. We present 3 additional OL cases involving the parotid, including a synchronous presentation with paraganglioma of the right carotid bifurcation. Microscopically, both the OLs were composed of a mixed population of oncocytes and adipocytes in varying proportions surrounded by a thin, connective tissue fibrous capsule. Oncocytes were positive for pan-cytokeratins (CKs) AE1/AE3, epithelial membrane antigen, CK5, CK7, CK14, CK18, and CK19. Calponin, p63, alpha-smooth muscle actin, and carcinoembryonic antigen were negative. Vimentin and S-100 protein were positive only in adipose cells. Despite distinctive morphologic features, OL is often misdiagnosed, given its rarity. We hope to contribute to surgeons’ and pathologists’ awareness and knowledge regarding the existence of this tumor and provide adequate management through conservative surgical excision.

Keywords

oncocytic lipoadenoma parotid gland salivary glands sialolipoma lipoadenoma

Introduction

Oncocytic neoplasms of the salivary glands represent a diverse group of tumors characterized morphologically by the predominance of oncocytic cells.^1-3 Except for Warthin's tumor, salivary gland tumors with oncocyte predominance are uncommon and include oncocytoma, oncocytic carcinoma (OCs), and oncocytic cystadenoma. However, other tumors can also exhibit oncocytic features such as pleomorphic adenoma, myoepithelioma, sialolipoma, mucoepidermoid carcinoma, and epithelial–myoepithelial carcinoma.^1,2,4-7

Recently, another oncocytic tumor affecting the salivary glands has been described and named oncocytic lipoadenoma (OL) or oncocytic adenolipoma.^2,8,9 The term oncocytic lipoadenoma, first coined in 1998 by Hirokawa et al,⁸ describes a rare morphologically distinct tumor composed of oncocytes and mature adipocytes. Currently, OLs remain poorly understood and have not yet been included in the current classification of World Health Organization head and neck tumors (2017) as a distinct clinicopathological entity.¹⁰ To the best of our knowledge, only 33 cases have been reported in the English-language literature to date,^2,8,9,11-24 including the current cases.

Herein, we report 3 additional rare OL cases affecting the parotid gland in conjunction with an extensive review of the literature to understand better the clinicopathological features of this uncommon salivary gland tumor.

Case Series

Case 1

A 60-year-old Caucasian female patient, nonalcohol drinker, and nonsmoker, referred to an oral medicine service presenting an extensive painless swelling in the left parotid region. The patient reported that she noticed the lesion 2 years earlier. Previous medical history included only arterial hypertension. A computed tomography scan was performed and showed a large, well-defined soft-tissue lesion with fat density arising from the superficial lobe of the left parotid gland. A fine-needle aspiration biopsy (FNAB) of the lesion was performed and revealed normal adipose tissue. Based on the imaging findings and FNAB results, a conservative surgical approach was performed. The lesion was removed by partial parotidectomy. On gross examination, the tumor was well defined, firm in consistency, predominantly yellowish with areas ranging from gray to brownish, and measuring 4.0 cm × 4.0 cm.

Morphologically, a tumor well-delimited by a thin fibrous capsule composed of oncocytes and adipose cells was observed. The oncocytes exhibited polygonal morphology, abundant granular, eosinophilic cytoplasm, and regular nuclei with dispersed chromatin and prominent central nucleoli permeated by adipose tissue. Mild inflammatory infiltrate composed of lymphocytes, and occasional plasma cells were also seen in association with the tumor component. By immunohistochemistry, oncocytic cells demonstrated positive staining for pan-cytokeratin (CK) AE1/AE3, CK7, epithelial membrane antigen (EMA), and CK5. Calponin, p63 and alpha-smooth muscle actin (α-SMA) were negative. The diagnosis was OL. At a clinical follow-up of 14 months, no recurrence was observed.

Case 2

An 81-year-old female was referred to a private service presenting with a right parotid tumor. The patient reported that she noted the lesion 3 months before the consultation. The tumor was asymptomatic and affected the superficial lobe of the parotid. During the clinical examination, a right cervical mass was also noted, which was surgically removed at the same time the right superficial parotidectomy was performed. The tumor was located at the bifurcation of the right carotid artery. Both lesions were asymptomatic. On gross examination, the parotid tumor was well circumscribed with smooth homogeneous, light brown, and yellow cut surfaces, measuring 5.0 cm in greatest dimension (Figure 1A). Morphologically, the tumor was well delimited by a thin capsule of fibrous connective tissue and composed of a mixture of oncocytes and adipose tissue (Figure 1B to D). By immunohistochemistry, the oncocytes were positive for pan-CKs AE1/AE3, EMA, CK5, CK7, CK14, CK8, CK 34βe12, and CK19 and negative for vimentin, p63, calponin, and α-SMA (Figure 2). The diagnosis was OL. The cervical tumor, morphologically, consisted of polygonal and spindle cells with nuclei round or oval and prominent nucleoli arranged in the Zellballen pattern (Figure 3A). Tumor cells were positive for chromogranin and synaptophysin (Figure 3B and C). Sustentacular cells were positive for the S-100 protein (Figure 3D). The diagnosis was carotid body paraganglioma.

Case 3

A 44-year-old male was referred to a private service presenting an extensive painless swelling in the right parotid region. On gross examination, the tumor was well circumscribed, firm in consistency, and yellowish with areas being brownish, and measuring 3.5 cm in its largest diameter (Figure 4A). Histopathologically, the tumor was well delimited by a fibrous capsule and composed of oncocytes and fat tissue. The oncocytes and adipocytes exhibited a normal appearance (Figure 4B to D). In immunohistochemistry, oncocytic cells were positive for pan-CK AE1/AE3, CK7, CK18, EMA, CK 34βe12, and CK5 and negative for p63, calponin, and α-SMA. The diagnosis was OL.

Discussion

The terms lipoadenoma and adenolipoma are used to refer to benign tumors composed of epithelial and lipomatous elements. These lesions have been described in various anatomical sites, including the breast, skin, thyroid, parathyroid, and salivary glands.^8,21,25-30 Interestingly, OLs seem to occur exclusively in the salivary glands, especially in the parotid gland (Table 1).

Table 1.

Summary of Cases of Oncocytic Lipoadenoma Previously Reported in the Literature, Including the Present Series (1998-2021).

Case	Author	Age (years)	Sex	Location	Size (cm)	% Fat component	Treatment	Recurrence	Follow-up (months)	Clinical status
1	Hirokawa et al⁸	66	Female	Submandibular gland	11.0	50	Submandibulectomy	No	30	ANED
2	Kato and Horie¹¹	57	Female	Parotid gland	4.4	40	Surgical resection	NR	NR	NR
3	Klieb and Perez-Ordoñez¹²	46	Female	Parotid gland	3.0	30-40	Superficial parotidectomy	No	6	ANED
4	Aouad et al¹³	38	Male	Parotid gland	4.0	NR	Total parotidectomy	NR	NR	NR
5	Chahwala et al¹⁴	50	Female	Parotid gland	13.5	NR	NR	NR	NR	NR
6	Ilie et al¹⁵	64	Male	Parotid gland	5.0	70	Parcial parotidectomy	No	24	ANED
7	Tokyol et al¹⁶^a	56	Male	Parotid gland	7.0	40	Total parotidectomy	No	6	ANED
8	McNeil et al¹⁷^a	70	Male	Parotid gland	4.2	40	—	—	NR	NR
9	Mitsimponas et al¹⁸	55	Female	Parotid gland	2.4	10	Lateral parotidectomy	No	12	ANED
10	Casadei et al¹⁹	NR	Male	NR	NR	30	Surgical resection	NR	NR	ANED
11	Casadei et al¹⁹	NR	Female	Submandibular gland	NR	30	Surgical resection	NR	NR	ANED
12	Casadei et al¹⁹	NR	Female	Parotid gland	NR	30	Surgical resection	NR	NR	ANED
13	Devadoss et al²⁰^a	50	Female	Parotid gland	13.5	50-60	—	No	24	ANED
14	Agaimy et al²¹	63	Male	Parotid gland	4.5	10	NR	No	6	ANED
15	Agaimy et al²¹	29	Male	Parotid gland	4.5	20	NR	No^b	141	ANED
16	Agaimy et al²¹	54	Female	Parotid gland	2.9	10	NR	No	18	ANED
17	Agaimy et al²¹	55	Male	Parotid gland	2.7	70	NR	No^c	13	ANED
18	Agaimy et al²¹	7	Female	Parotid gland	NR	50	NR	NR	NR	NR
19	Agaimy et al²¹	89	Male	Parotid gland	4.2	80	NR	NR	NR	NR
20	Lau and Thompson²	61	Male	Parotid gland	2.0	20	Superficial parotidectomy	No	42	ANED
21	Lau and Thompson²	83	Male	Parotid gland	2.5	15	Superficial parotidectomy	No	12	ANED
22	Lau and Thompson²	67	Male	Parotid gland	4.0	5	Superficial parotidectomy	No	3	ANED
23	Lau and Thompson²	40	Female	Parotid gland	4.0	50	Superficial parotidectomy	No	148	ANED
24	Lau and Thompson²	56	Male	Parotid gland	3.5	70	Superficial parotidectomy	No	110	ANED
25	Lau and Thompson²	65	Male	Parotid gland	1.9	50	Superficial parotidectomy	No	57	ANED
26	Lau and Thompson²	65	Male	Parotid gland	3.5	50	Superficial parotidectomy	No	26	ANED
27	Ashraf et al²²	56	Female	Parotid gland	3.0	NR	Superficial parotidectomy	NR	NR	NR
28	Parmar²³	45	Male	Submandibular gland	6.0	NR	Surgery	NR	NR	NR
29	Çelik et al²⁴	36	Male	Submandibular gland	2.9	NR	Submandibular gland excision	NR	NR	NR
30	Shakya and Nepal⁹	46	Male	Parotid gland	15.0	NR	Surgery	No	60	ANED
31 (case 1)	Present series	61	Female	Parotid gland	4.0	60	Superficial parotidectomy	No	14	ANED
32 (case 2)		81	Female	Parotid gland	5.0	60	Superficial parotidectomy	NR	NR	NR
33 (case 3)		41	Male	Parotid gland	3.5	60	Superficial parotidectomy	NR	NR	NR

Abbreviations: NR, not reported; ANED, alive with no evidence of disease.

The full text was not available.

The patient had a periparotideal lipoma resected from the same site 20 months ago.

The patient had a history of sinonasal adenocarcinoma treated by surgery and irradiation 26 months before the diagnosis of oncocytic lipoadenoma.

An English-language literature review on OLs revealed only 33 cases reported to date, including the current cases (Table 1). This tumor occurs in a wide age range, affecting children to the elderly (range: 7-89 years), with a mean age of 54.6 years (SD ± 16.1). OL has a slight male predilection, with a male-to-female ratio of 1.4:1. Clinically, it usually presents as a painless, slow-growing mass or swelling with a long evolution time. Most cases arise in the parotid gland, with only 4 previously reported involving the submandibular gland.^8,19,23,24 To date, no cases were reported in the minor salivary glands. These tumors seem to have a benign clinical course with nonaggressive behavior. So far, no recurrence has been reported (mean follow-up of 39.6 ± 45.1 months).^2,8,9,11-24

On macroscopic examination, OLs are well-circumscribed tumors.^2,21 The cut surface's coloration varies from brown to yellowish, depending on the amount of adipose tissue present in the lesion,^2,9 similar to the current cases. Morphologically, the tumors generally are encapsulated by a thin fibrous capsule. Two different cellular components are observed: oncocytes and adipocytes. The oncocytic cells are usually organized in larger clusters or nests and acini with a morphological appearance similar to a conventional oncocytoma. The tumor's fatty component has the appearance of normal adipocytes and it comprises about 5% to 80% of the tumor volume.^2,8,9,11-24 In addition, foci of typical salivary gland elements, including ducts, serous acini, and sebaceous glands, and mild lymphocytic inflammatory infiltrate associated with the tumor are frequent findings in OLs.^2,12

Both adipose and oncocytic components can predominate in some regions of the tumor. Therefore, this finding should be considered when performing a fine-needle biopsy.² Although samples collected by fine-needle aspiration are of little accurate help in the diagnosis of these lesions, and several cases have been misdiagnosed, such as oncocytomas, lipomas, pleomorphic adenomas, and acinic cell carcinoma with oncocytic features,^12,14,20 cytologically, the exclusive presence of a prominent oncocytic epithelial component in a lipoid background should favor the cytological diagnosis of OL.¹⁴

The morphological features of OL are sufficiently distinctive and allow diagnosis on sections stained with routine hematoxylin and eosin.² Although immunohistochemical analysis is usually not necessary for the diagnosis, the immunophenotype of OL has been reported previously.^{11, 12,15-17,20} The oncocytic cells express pan-CK AE1/AE3, CK7, and EMA. Positivity for p63, CK5/6, CK14, CK19, and high-molecular-weight keratins (34βe12) are observed in basal cells.^12,15,17 Tumor cells are negative for muscle markers such as calponin, α-SMA, and muscle-specific actin (HHF35),^12,15-17,20 findings similar to our cases.

The main morphologic differential diagnoses include other oncocytic neoplasms that exhibit a prominent oncocytic component.² Among the lesions, OL is most commonly confused with oncocytoma. Although both tumors are well circumscribed and composed of classic oncocytes, oncocytomas lack the adipose component characteristic of OL. The presence of fat tissue aids in distinguishing between Warthin's tumor with nodular oncocytic proliferation, stroma-poor Warthin's tumor, and pleomorphic adenoma with oncocytic features from OL.² OL also may be confused with OCs; however, OCs are very rare. Their absence or low frequency in many large salivary gland tumor series^31,32 has raised doubts about the existence of true OCs or whether these lesions may represent variants of other carcinomas, such as microsecretory or ductal adenocarcinomas with prominent oncocytic findings.

However, nodular oncocytic hyperplasia presents multifocal nests of oncocytes mixed with normal-looking fat cells and acinar cells^14,33 and may mimic an OL.² However, OLs are well-circumscribed encapsulated tumors by a thin fibrous capsule. In contrast, nodular oncocytic hyperplasia is an unencapsulated proliferation of oncocytes with a frequent multifocal distribution.^2,14,33 Differential diagnosis also includes sialolipomas, a rare histological variant of the lipoma composed of adipocytes and normal salivary gland tissue.⁴ Although epithelial/myoepithelial elements of sialolipomas may exhibit focal oncocytic metaplasia in some cases, in general, it does not have a prominent oncocytic component such as OLs. In addition, sialolipomas tend to exhibit multiple lobes of fat tissue, with the salivary gland elements uniformly distributed within the fatty component.^2,4

Interestingly, tumors exhibiting both characteristics of OL and sialolipoma have been illustrated by other investigators and described as “oncocytic sialolipomas.”^21,34 Pusiol et al³⁴ reported an interesting case of a probable sialolipoma affecting the submandibular gland with a prominent oncocytic component. We believe that this case may represent an oncocytic adenolipoma instead of an oncocytic sialolipoma. Although oncocytic metaplasia can occur in sialolipomas, this component tends to be focal, different from what seems to occur in the case reported by Pusiol et al.³⁴ However, more representative photomicrographs of the lesion would be necessary to confirm the diagnosis. Some cases showing discrete areas similar to sialolipomas within a typical OL have also been reported.² It remains to be determined whether these lesions should be classified as oncocytic sialolipoma, OL, or a hybrid tumor. However, the existence of phenotypically mixed cases suggests a possible histogenetic relationship between both the lesions.²

Interestingly, the patient of case 2 also presented with a synchronous paraganglioma involving the right carotid bifurcation. Paragangliomas are rare catecholamine-secreting endocrine tumors.³⁵ About 80% of the head and neck region's paragangliomas occur in the carotid body and jugular fossa, similar to the current case.³⁶ The simultaneous presentation of paraganglioma and OL is a rare event. To the best of our knowledge, this is the first synchronous case of paraganglioma and oncocytic adenolipoma reported in the literature. The association between these 2 entities is misunderstood, and the existence of common etiological factors for both entities remains unclear.

The pathogenesis behind OL development remains unclear.^2,9 Some authors argue that these tumors represent an oncocytoma with extensive lipomatous metaplasia. Adipocytic differentiation in salivary gland pleomorphic adenomas has been attributed to the transdifferentiation of myoepithelial cells, which results in a metaplastic transition to adipocytes.³⁷ However, immunohistochemical and ultrastructural studies have not demonstrated myoepithelial cells’ presence in OL.^{11,12,15-17,20} Interestingly, a group of peripheral basal cells has been shown to be immunopositive for p63 and basal-like keratins in OLs.^12,15-17 Although it is speculative, and the exact nature of this cell population is still unclear, these could represent basal cells or pluripotent stem cells capable of undergoing lipomatous metaplastic alteration.²

Cytogenetic analysis of OL showed a t(12;14) translocation involving the high-mobility group AT-hook 2 (HMGA2) gene on chromosome 12.¹⁵ HMGA2 encodes a protein that belongs to the nonhistone high-mobility group protein family. This protein influences several cellular processes by regulating gene transcription.³⁸ HMGA2 gene rearrangements were also recognized in several neoplasms, including lipomas and a subset of pleomorphic adenomas.^39,40 Further molecular studies may yield more concrete evidence regarding the importance of HMGA2 gene disruption in OL emergence and development.²

Regarding the treatment of OLs, most of the parotid gland tumors have been treated by total or superficial parotidectomy,^2,12-14 similar to the current case. Despite the lack of follow-up data in some cases,^9,21-24 no recurrence has been reported so far.

In summary, OLs are rare salivary gland tumors. Although they have a classic morphological appearance that allows an accurate diagnosis based only on hematoxylin and eosin evaluation, they are often misdiagnosed with other salivary gland tumors with a prominent oncocytic component. Clinically, OL has a benign clinical course and no risk of recurrence after complete surgical excision.

Footnotes

Acknowledgments

This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). The author John Lennon Silva Cunha received a PhD scholarship from CNPq.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Informed Consent

Not applicable, because this article does not contain any studies with human or animal subjects.

Trial Registration

Not applicable, because this article does not contain any clinical trials.

ORCID iD

John L.S. Cunha

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