Basal Cell Adenocarcinoma of the Parotid Gland in an Elderly Iranian Woman and Review of the Literature

Basal Cell Adenocarcinoma (BCAC) is one of the rare subtypes of carcinoma of salivary glands. It is a salivary gland malignancy that was first recognized as a distinct neoplastic entity in World Health Organization’s (WHO’s) classification of salivary gland tumors in 1991. BCAC of the salivary gland is a rare neoplasm, especially in the parotid gland. It composes 1.6% of all salivary gland neoplasms and 2.9% of malignant salivary gland neoplasms. The most important differential diagnosis of BCAC is Basal Cell Adenoma (BCA), but the behavior of BCAC is invasive and destructive with perineural and vascular invasion [1,2]. The histopathology of BCAC shows two cell types, i.e., small basaloid epithelial cells at the periphery and larger epithelial cells in the center of the tumour clusters . Most cases of BCAC are de novo, but 25% of BCACs originate from pre-existing basal cell adenomas. In general, BCAC has a good prognosis. Metastasis is rare but may recur locally [3,4]. BCACs are categorized into four types on the basis of their growth patterns, i.e., solid, trabecular, tubular, and membranous; the solid type is the most common [2,5]. The BCAC in our 71-year-old patient had some interesting features that were different from those in previous case reports.

A 71-year-old Iranian woman with a 30-year history of a large mass on the right side of her neck was referred to the Otolaryngology Department at Shahid Sadoughi Hospital in Yazd, Iran in 2012. She presented with a firm, fixed, non-tender mass on the right side of her neck that measured 10×15 cm with normal skin with no apparent invasion. The clinical examination provided no evidence of cervical lymphadenopathy. The patient complained about mild dysphagia, and the oropharyngeal exam revealed a bulging mass in the right side of the oral cavity. Facial movements were partially asymmetrical on the right side of the lower lip (other branches of facial nerve were intact). Also, a bulge was found on the anterior wall of the right external auditory canal. A superficial parotidectomy was performed 10 years ago; subsequently, the patient experienced five recurrences of masses on her neck, and the last recurrence occurred four years ago. Unfortunately, we don’t have any documented pathology from her previous surgeries. An investigation of the patients’ family history showed no occurrence of cancer.

Investigation

Imaging

Abdominal ultrasonography revealed no abnormality, and the chest X-ray indicated no signs of metastasis. The CT scan showed a large, irregular mass in the right parotid gland, bulging into the parapharyngeal space. It extended up to the base of the skull (Figure 1).

Figure 1: Mass extension in patient axial cut of neck CT scan

Histopathology and other laboratory findings

In the gross pathological examination, the tumour had creamy-colored nodular tissue that measured 16×14×5 cm with firm consistency and lobular appearance in the cut section. Some of nodules had thin capsules with calcified foci. Microscopic examination revealed a tumoural lesion with a multinodular pattern composed of basaloid cells that had round-to-oval nuclei with fine nucleoli and scant-to-moderate cytoplasm. Cells arranged in lobules, sheets, aggregates cords, trabeculae and membranous pattern. Hyaline Periodic Acid Schiff (PAS) positive materials with palisading and jigsaw puzzle patterns were observed. There were no more than six mitoses in the 10 High Power Field (HPF).

Cellular pleomorphism, necrosis, vascular and perineural invasion, and lymph node metastasis were absent. The primary diagnosis was low-grade basal cell adenocarcinoma. For ruling out other differential diagnoses, Immunohistochemistry (IHC) was performed. The tumoral cells were positive for CK AE1/3, SMA, S100 (moderately positive), EMA and CD117 (positive in luminal cells in areas of ductal differentiation), Vimentin (focally positive), and Ki67 (in 5 to 10% of the tumoral cells). CEA and GFAP were negative (Figures 2 and 3) (Table 1).

Figure 2: EMA immunostaining positive in luminal cell in areas of ductal differentiation

Figure 3: ASMA immunostaining positive in abluminal cells.

Table 1: Antibodies used in the immunohistochemical investigation of BCAC

The tumor at the base of the skull and the deep portion of the parotid gland were resected, and suprahyoid dissection of the lymph nodes was performed, including the submandibular, submental, and upper third of the jugulodigastric nodes. Except marginal mandibular branch the facial nerve was preserved and post-operative irradiation were conducted.

Outcome and follow-up

At the one-year follow up, she had no recurrence of any of the features associated with bcac. Also, the metastasis workup revealed no sign of metastasis.

Bcac is slow-growing, locally-destructive tumor. It was first defined as a malignant tumor of the salivary gland in 1991. The most important differential diagnosis for bcac is basal cell adenoma [1]. Both of them have similar histological appearances (basaloid pattern), but infiltrative growth is the distinguishing feature of bcac. Pathological criteria for the diagnosis of bcac include infiltrative growth with vascular or perineural invasion. Other features may include nuclear pleomorphism, necrosis, and mitotic activity [3,4]. In our patient, there were no more than six mitoses inthe 10 hpf. Cellular pleomorphism, necrosis, vascular and perineural invasion, and lymph-node metastasis were absent, but, clinically, it was a huge mass (10×15 cm) with wide extention and a history of multiple recurrences. Its invasion of the adjacent soft tissues was obvious during surgery. Ihc suggested bcac and ruled out a differential diagnosis. We believe that the diagnosis of bcac is clinicopathological, and sometimes it is very difficult to distinguish it from basal cell adenoma using only pathological criteria.

The rate of metastasis is low, but the rate of local recurrence is high. Metastasis occurs in less than 10% of cases, and only one case involving the lung has been reported [3,4]. Because of their biological behavior and their prognosis, bcacs should be classified as low-grade carcinomas. In our patient, a complete metastasis workup was performed, and there were no features of metastasis. There have been a few descriptions of facial paralysis or additional destruction of the salivary gland, but interesting findings in our patientâ€^™s case were that the buccal branch of the facial nerve was weak and that the bcac extended up to the base of the skull, bulging into the parapharyngeal space. Many patients with bcac recognized after 7-10 years, but our patient had it for the long duration of about 30 years with five recurrences (may be denovo or transformation of basal cell adenoma). Most patients present with a solitary firm nodule between 1 and 3 cm that is slowly enlarging. The largest tumor described by Ellis et al. was 4 cm, but our patient’s tumor was about10x15 cm. Local recurrence occurs in about one-third of the cases, and our patient had five recurrences over a 30-year period. Our case was unique with respect to its duration, the number of recurrences, and the size of the mass [5].

Bcac has four subtypes, i.e., solid, membranous, trabecular, and tubular. The solid areas of bcacs are composed of nonluminal cells, some of which contain tonofilaments and well-formed desmosomes; tubulo-trabecular differentiated into both luminal and nonluminal cells. Both growth patterns were associated with the formation of excess basal lamina, marginally and between nonluminal cells. The majority of these tumors are solid. They are characterized by islands and masses within the fibrous connective tissue stroma, the histological type of our patients bcac was membranous. The membranous type is actually the second most frequently-occurring type of bcac, accounting for about 20% of all occurrences. This type has thick, eosinophilic, periodic acid schiff positive hyaline laminae that surround and separate one tumor nest from another and a jigsaw puzzle formation (Figure 4). The trabecular type of bcac has anastomosing cords of basaloid epithelial cells that look like chinese characters [2,5].

Figure 4: Lobules with jigsaw puzzle like pattern in Membranous BCAC

Muller and Barnes conducted an extensive literature search in 1996, and they concluded that parotid is the most common salivary gland that is involved with BCAC (89% in the parotid, 10% in the submandibular gland, and 1% among the minor salivary glands). In our case, the parotid gland was involved. Most studies recommend wide loc al excision. Treatment for regional metastasis (neck) is done for significant lymphadenopathy on clinical or radiologic examination, and postoperative radiation is recommended for close surgical margins or following surgical excision of recurrent tumor [6-9].

The surgical procedure we performed was resection of the tumor at the base of the skull with deep portion resection of the parotid gland with preservation of the facial nerve. At last we summarise at least 46 cases of parotid gland BCAC from 1990-2014 in two tables and compare them with our case (Tables 2 and 3).

Table 2: Review of the literature

Table 3: Review of the literature