Ceruminous adenoma of the external auditory canal: 9 cases series with imaging and pathologic findings

Objectives Ceruminous adenoma is a rare benign tumor of the external auditory canal. This study aimed to present the clinical characteristics, imaging findings, pathological results and the management outcomes of the ceruminous adenoma. Study design Retrospective case series review. Setting Tertiary referral center. Patients and methods Patients undergoing surgery for ceruminous adenoma of the external auditory canal between the years 2004 to 2018. All patients with ceruminous adenoma were analyzed for demographic, clinical, radiological features and pathologic findings. The outcomes of the management were also evaluated. Results Nine patients with ceruminous adenoma were included in the study. Hearing loss was the most common complaint (5/9, 56%), followed by otalgia (4/9, 44%), pruritus (4/9, 44%), and otorrhea (2/9, 22%). The tumors originated mostly from the cartilaginous portion of the external auditory canal (8/9, 89%) and merely from the bony portion of the external auditory canal (1/9, 11%). Pathohistological study indicated that the ceruminous adenomas were divided into three types: the ceruminous gland adenoma (6/9, 67%), the ceruminous pleomorphic adenoma (2/9, 22%) and the ceruminous syringocystadenoma papilliferum (1/9, 11%). No recurrence was found during follow-up for two to fifteen years after surgical resection. Conclusion Ceruminous adenomas are rare entities. They originate mainly from the cartilaginous portion of the EAC, but occasionally from the bony portion of the EAC. The surgical section with enough margin is adequate for management of these tumors.


Introduction
Ceruminous glands are modified apocrine glands located primarily in the outer one-third to one-half of the external auditory canal (EAC). Ceruminous gland tumors of the EAC are very rare clinical-pathological entities (1). The benign tumor of the ceruminous glands is also referred to as 'ceruminous adenoma (CA)', which shows a dual population of a basal, myoepithelial layer surrounding inner luminal secretory cell (2,3) and is usually separated into three types, based on histologic features: ceruminous gland adenoma, ceruminous pleomorphic adenoma, and ceruminous syringocystadenoma papilliferum (1,4,5). CA has a good prognosis after complete excision. The literature on these tumors is limited to case reports and small group cases, and there is a lack of comprehensive evaluation. We present herein 9 cases of ceruminous adenomas at a tertiary care center and briefly describe the salient clinical data, imaging findings, pathological features, treatment modalities, to raise awareness of this rare entity.

Methods
Following Institutional Review Board approval from Beijing Tongren hospital, a retrospective chart review was performed to identify all patients with histologically confirmed ceruminous adenoma between 2004 and 2018. Nine patients diagnosed with ceruminous adenomas of the EAC were found. The following data were extracted: patient demographics, presentation, imaging, histopathology, treatment, follow-up, recurrence, and final outcome of disease.

Radiographic findings
High-resolution computerized tomography (HRCT) was obtained for 8 of 9 patients and magnetic resonance imaging (MRI) was acquired for 7 of 9 of the patients. All patients demonstrated a soft mass in the EAC. The masses ranged in size from 4 to 36 millimeter in greatest dimension (mean, 17 mm). The site of the tumors is summarized as follows: in six cases (6/9, 67%) the lesions were located only in the cartilaginous portion of the external auditory canal (EAC); in one case (1/9, 11%) the lesion was located only in the bony portion of the external auditory canal (EAC) ( Figure 1); in one case (1/9, 11%) the lesion was originated from the cartilaginous portion with extension into the bony part of the EAC; in another case (1/9, 11%), the tumor located in the cartilaginous portion and protruded out from the EAC. The tumor margin was well circumcised and confined in all cases. On temporal HRCT, all of the lesions exhibited isoattenuating soft tissue masses in the EAC, one mildly involved the tympanic bone ( Figure 1). In one patient several calcification foci were found in the mass, and the mass showed heterogenous enhancement on the CT with the soft window. Seven cases were examined with MRI, six cases underwent contrast-enhanced MRI, and DWI was performed in five cases. On Figure 2 showed that the tumor was adjacent to the parotid gland, however, the Figure 2F revealed the tumor was originated in the EAC, there was a gap between the tumor and the parotid gland, and Figure 2G revealed the integrity of the tumor capsule. Thus, the tumor did not contain any salivary gland tissue, and the tumor originated in the EAC (See Table 2).

Histology
On gross appearance, 6 lesions appeared as solid masses, 3 cases appeared as cystic-solid masses; the masses were round, ovale, or lobulated. According to the 2017 WHO classification of ceruminous neoplasms, nine cases were diagnosed as benign ceruminous adenoma. Among them, six cases were diagnosed as ceruminous gland adenoma ( Figure 3A), two cases were diagnosed as ceruminous pleomorphic adenoma ( Figure 3B), one case was diagnosed as ceruminous syringocystadenoma papilliferum ( Figure 3C).

Treatment
Seven patients were operated under general anesthesia and two patients were operated under local anesthesia. Six patients underwent endaural microscope surgery, two patients underwent transcanal endoscope surgery, and one patient underwent postauricular approach surgery. Postaural free skin flaps were used in seven patients. No recurrence was found in all patients during the follow-up from 3 to 17 years.

Discussion
Ceruminous glands are modified apocrine glands located mainly in the skin lining cartilaginous portion of the external auditory canal (EAC) (2). The medial bony portion of the EAC is normally free from these glands, although they can be seen rarely as an incidental finding.
Ceruminous adenomas develop mainly in the cartilaginous portion of the external auditory canal, rarely in the osseous portion (6,7). In our series, eight cases of ceruminous adenoma originated from cartilaginous portion of the EAC, only one case originated from bony portion of it ( Figure 1).
The typical symptoms of ceruminous adenoma, such as conductive hearing loss, otorrhoea and pain, are usually related to the size of the lesion and the degree of canal obstruction. It's also entirely possible that squamous epithelial keratin debris could accumulate behind the mass leading to the problem of cholesteatoma. The benign adenoma may exist for many years. The longest disease duration before admission in our series is seventeen years. Ceruminous adenoma is typically a skincovered, round or ovale, polypoid or lobulated mass of variable size in the EAC. It may demonstrate a cystic to solid pattern. In our series, 6 cases present as solid mass, 3 cases present as cysticsolid mass.
CT as a routine examination can determine the exact location of the tumor and evaluate whether there is bone destruction or not. On  CT examination ceruminous adenomas usually present as a soft mass. In our series there was no tympanic bone destruction in all cases except one case, in which only mild bone destruction was found. Calcification foci were found in one of our cases with ceruminous pleomorphic adenoma (Figures 2A, B). Calcification in ceruminous adenoma was not reported in the literature. The calcification is thought to be a result of long-term tumor progression in pleomorphic adenoma of other sites. The frequency of calcification was 50% in parapharyngeal space pleomorphic adenoma and 15% in parotid pleomorphic adenoma (8,9). MRI can determine the extent and margin of the tumor. Ceruminous adenoma usually demonstrated a well-circumicised mass without infiltration to adjacent tissue. In one of our cases the tumor growed adjacent to the parotid but showed no infiltration. They might show intermediate, high or low signal intensity on T1WI, and show intermediate or high signal intensity on T2WI. They may show homogenous, or heterogenous, or edge enhancement. On DWI they showed as intermediate signal, but cholesteatoma behind the tumor appeared as high signal ( Figure 2E).
The benign tumors of ceruminous gland are separated into three histologic types: ceruminous adenoma, ceruminous pleomorphic adenoma, ceruminous syringocystadenoma papilliferum. All these tumors are unencapsulated, but are usually well circumscribed or defined (5). The overlying surface epithelium is usually not involved. They showed no infiltration to other tissue.
Ceruminous gland adenomas (CGA) are the most common benign glandular tumors of the EAC. The lesion consists of glandular structures lined by two-layers of epithelium typically arranged in lobulated clusters ( Figure 3A). The inner luminal secretory cells display abundant eosinophilic cytoplasm with scattered yellowish-brown ceroid cytoplasmic pigment granules, while the myoepithelial cells line up along the basement membrane. Cystic and solid pattern of growth may be present.
Ceruminous pleomorphic adenoma (CPA), also referred to as mixed tumor, is the second most common benign glandular neoplasm of the EAC. It is characterized by a mixed cellular presence consisting of the epithelial cells lining the lumens of tubular formations surrounded by nests of myoepithelial cells within a myxochondroid or even mucoid matrix ( Figure 3B) (10,11). Myoepithelial cells of the ceruminous glands are thought to be the precursor of primary pleomorphic adenoma of the ear canal. Ceruminous pleomorphic adenoma is identical to salivary gland pleomorphic adenoma, requiring careful exclusion of extension from a primary parotid gland tumor into the EAC.
Ceruminous syringocystadenoma papilliferum is an extremely rare lesion in the EAC, only a dozen of cases were reported (12)(13)(14)(15)(16). It specifically contains papillae lined by two-layered epithelium projecting into cystic lumens ( Figure 3C). Luminal cells usually reveal prominent apical caps with decapitation secretion, typical of the ceruminous glands. It contains solid and cystic areas.
The mainstay in the management for all benign ceruminous gland tumors of the external ear canal is en bloc surgical resection with a negative margin (5). Transmeatal excision is usually adequate for small tumors, while postauricular approach may be needed for larger tumors. A free skin flap is usually recommended for reconstruction. The possibility of recurrence for these benign tumors seems to be related only to an incomplete surgical excision of the lesion (17). Although the recurrence rate is low, long-term follow-up is needed. Radiation and chemotherapy are not used to treat these benign neoplasms.

Conclusion
Ceruminous adenomas are benign tumors of the EAC. They are rare entities. They originate mainly from the cartilaginous portion of the EAC, but occasionally from the bony portion of the EAC. The ceruminous gland adenoma is the most common histologic type of benign glandular neoplasms, the ceruminous pleomorphic adenoma is the second most common of these neoplasms, and the ceruminous syringocystadenoma papilliferum is an extremely lesion in the EAC.Calcification can be found in the large ceruminous pleomorphic adenoma. The surgical section with enough margin is adequate for management of these tumors.

Data availability statement
The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

Ethics statement
The studies involving human participants were reviewed and approved by Ethics Committee of Beijing Tongren Hospital, Capital Medical University. The patients/participants provided their written informed consent to participate in this study. Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.