
==== Front
J Cytol
J Cytol
JCytol
J Cytol
Journal of Cytology
0970-9371
0974-5165
Wolters Kluwer - Medknow India

JCytol-41-166
10.4103/joc.joc_184_23
Original Article
Fine-needle Aspiration Biopsy of Pilomatrixoma (Cytological Features of Six Cases Histologically Approved)
Ozcan Burcu 1
Erdogan-Durmus Senay 2
1 Department of Pathology, İstanbul Training and Research Hospital, Cytopathology Division, İstanbul, Turkey
2 Department of Pathology, Prof. Dr. Cemil Tascioglu City Hospital, Cytopathology Division, İstanbul, Turkey
Address for correspondence: Dr. Senay Erdogan-Durmus, Prof. Dr. Cemil Tascioglu City Hospital, Department of Pathology, Cytopathology Division, Şişli, İstanbul, Turkey. E-mail: senayerdgn@gmail.com
Jul-Sep 2024
18 7 2024
41 3 166170
01 11 2023
05 4 2024
05 6 2024
Copyright: © 2024 Journal of Cytology | Indian Academy of Cytologists
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Background and Objective:

Pilomatrixoma is a rare, benign, slow-growing tumor of the hair matrix. Excisional biopsy is often the preferred method of diagnosis for cutaneous masses including pilomatrixoma. However, fine-needle aspiration is also performed on these lesions. There are very few reports on the cytologic features of pilomatrixoma in fine-needle aspiration. In this study, we aimed to evaluate the clinical and cytological features of six cases of pilomatrixoma, which were confirmed histopathologically.

Materials and Methods:

The study includes six cases of pilomatrixoma, which were diagnosed by two cytopathologists in 2019 and 2022. A detailed cytological analysis was done by a semiquantitative method. Cellularity, basaloid cells, squamous cells, giant cells, shadow cells, naked nuclei, calcium deposits, inflammation, and debris were semiquantified from 0 to 3+.

Results:

The ages of patients ranged from 8 to 63 years old. The male-to-female ratio was 2:1. All cases occurred in the head and neck area. The cytological diagnosis was pilomatrixoma in five cases and epidermoid/dermoid cyst in one case. The surgical excision was performed in all patients. The diagnosis of pilomatrixoma was confirmed histologically in all cases.

Conclusıon:

Fine-needle aspiration biopsy (FNAB) of pilomatrixoma can be a diagnostic challenge. There are very few reports on the cytologic features of pilomatrixoma in FNAB smears. The presence of ghost cells and basaloid cells should suggest the possibility of pilomatrixoma. The presence of giant cells, fibrillary matrix, calcium deposits, squamous cells, naked nuclei, inflammation, and debris are cytological findings supporting the diagnosis.

Basaloid cells
FNAB
pilomatrixoma
shadow cells
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pmcINTRODUCTION

Pilomatrixoma (PMX) is a rare, benign, slow-growing tumor of the hair matrix.[1] It accounts for approximately less than 1% of all benign skin tumors.[2] It was first described as “calcifying epithelioma of sebaceous gland” by Malherbe et al.[3] in 1880. In 1961, Forbes and Helwig replaced this term with PMX, which describes the histogenesis of the tumor from the hair matrix and cortex.[4]

PMX usually presents as a solitary, hard, intradermal, or subcutaneous nodule with predilection for the head and neck, and upper extremities with predominance in female patients.[15] It is usually small-sized, varying from 1 to 3 cm in diameter.[16] It usually occurs in the first decades of life.[5] However, PMX may occur at any age and may have an unusual clinical presentation such as large size, deep localization, or multicentricity.[7]

Histologically, the tumor is often surrounded by a fibrous capsule and composed of uniform basaloid cells and shows squamous differentiation and degeneration centrally, leaving anucleated cells (ghost or shadow cells).[5]

Fine-needle aspiration (FNA) is a simple, fast, safe, and useful method being used fort he diagnosis of various neoplasms.[56] PMX occurring in the head and cervical region may be difficult to clinically differentiate from enlarged cervical lymph nodes, salivary gland neoplasms, or other skin adnexal tumors. FNA is often performed to determine the nature of these cervical masses.[8]

In this study, we aimed to evaluate the clinical and cytological features of six cases of PMX, which were confirmed histopathologically.

MATERIALS AND METHODS

The study includes six cases of PMX, which were diagnosed by two cytopathologists in 2019 and 2022. In all cases, the aspirations were done with a 25 G needle.

Cytological preparation

The conventional slides were stained with May-Grünwald-Giemsa (MGG) stain (5 min with May-Grünwald and 15 min with Giemsa) and Papanicoalaou (PAP) stain.

In all cases, slides were prepared by using the liquid-based cytology (LBC) technique. For LBC slides, SurePath pap test kit (BD Diagnostics-tripath, Burlington, NC, USA®) was used. The samples in ethanol-based fixative were centrifuged twice. After the vortex of the material, the samples were spread as a thin layer in a circular area of the microscope slides and stained with PAP.

The cell blocks were obtained (in all cases) by the formaldehyde-alcohol and/or plasma-thrombin method.

Cytopathological assessment

A detailed cytological analysis was done by a semiquantitative method. Cellularity, basaloid cells, squamous cells, giant cells, shadow cells, naked nuclei, calcium deposits, inflammation, and debris were semiquantified from 0 to 3+ (0: absent, 1+: mild, 2+: moderate, and 3+: abundant).

Statistical analysis

Data analysis was performed using the SPSS 25.0 program (IBM®). In the evaluation of results, descriptive statistics were shown in the form of mean ± standard deviation, and nominal variables were shown as the number of cases and the percentage (%). Compliance normal distribution of numerical values was analyzed by the Shapiro–Wilk test.

RESULTS

The ages of patients ranged from 8 to 63 years old. The male-to-female ratio was 2:1. All cases occurred in the head and neck area. Clinical characteristics and duration of the lesions are summarized in Table 1. The cytological diagnosis was PMX in five cases and epidermoid/dermoid cyst in one case. The surgical excision was performed in all patients. The diagnosis of PMX was confirmed histologically in all cases.

Table 1 Demographic data, lesion locations, sizes, duration, clinical findings, cytologic diagnosis of case

Case no.	Sex/age (years)	Location	Size (cm)	Duration (months)	Clinical characteristics	Cytologic diagnosis	
1	M/63	Nose	0,8	8	Mobile, firm	Pilomatrixoma	
2	M/34	Neck	4,7	5-6	Mobile, firm	Pilomatrixoma	
3	F/54	Neck	2,2	24	Mobile, tender	Pilomatrixoma	
4	F/22	Posterior auricular	0,9	4-5	Fixed, tender	Inclusion cyst	
5	M/8	Scalp	1,6	6	Mobile, firm, tender	Pilomatrixoma	
6	M/24	Preauricular	1,3	6	Fixed, tender, erythematous	Pilomatrixoma	

The cytological features of the cases are shown in Table 2.

Table 2 The cytological features of the cases

Case No.	Cellularity	Basaloid cells	Squamous cells	Shadow cells	Giant cells	Naked nuclei	Calcium deposits	Inflammation	Debris	
1	2+	1+	1+	3+	0	1+	0	0	1+	
2	2+	1+	1+	2+	0	0	0	2+	3+	
3	2+	2+	1+	2+	0	0	0	2+	1+	
4	1+	0	2+	2+	0	0	0	0	1+	
5	2+	3+	1+	1+	3+	2+	1+	1+	2+	
6	3+	3+	2+	3+	1+	3+	0	1+	1+	

Cellularity: With the exception of case 5, the smears contained moderate to high numbers of cells with basaloid cells, squamous cells, and giant cells.

Basaloid cells: All aspirates showed tightly arranged clusters of basaloid cells. These cells were small-medium sized with round to oval nuclei and scant cytoplasm. Their chromatin was evenly dispersed and nucleoli were prominent in one of the cases (case 6) [Figures 1 and 2]. In some of cases many of these cells lacked cytoplasm completely and were represented by naked nuclei (cases 6 and 7). The individual cells were surrounded by a thin, fibrillary, pink (in MGG), matrix-like material in one of the cases (case 5, Figure 2).

Figure 1 (a-c) Tightly arranged clusters of basaloid cells. (a, b) MGG ×1000, (c) MGG ×400), (d-f) foreign body type giant cells. They are often attached to a basaloid cell cluster (d). (d, e: MGG ×400, f: MGG ×1000), (g-i) plaques of anucleated ghost cells (g: MGG ×200, (h) MGG ×400, (i) MGG ×1000)

Figure 2 (a) Loose clusters of basaloid cells and naked nuclei with prominent nucleoli. Note the presence of squamous cells. (MGG ×1000), (b) tumor cells surrounded by a thin, fibrillary, pink (MGG), matrix-like material. (MGG ×400), (c) cluster of basaloid cells with a keratinized squamous cell (PAP ×1000), (d) dispersed basaloid cells with naked nuclei and a squamous cell (PAP ×1000), (e) tumor cells, calcification, and inflammation in the background (PAP ×1000). (f) Nucleated and anucleated squamous cells (PAP ×200)

Squamous cells: Squamous cells with small, dark nuclei and dense cytoplasm were observed but were less evident. Anucleated squamous cells were prominent in one of the cases, and this case was misdiagnosed as an epidermoid/dermoid cyst (case 4) [Figure 2].

Shadow cells: Sheets of ghost cells could be identified in all FNAs. They occurred in medium-sized and large sheets of pale, non-nucleated cells [Figures 1 and 3].

Figure 3 Appearance of shadow cells, small areas of debris, and basaloid cell clusters on liquid-based cytology slides (a, c: PAP ×200, b, d: PAP ×400, LBC)

Giant cells: Multinucleated giant cells were found in two cases (cases 5 and 6). They were foreign body type and were often attached to a basaloid cell cluster [Figure 1].

Other findings: All smears contained cell debris in different amounts [Figures 1 and 3]. Inflammatory cells also were observed frequently. Calcium deposits were observed in only one of the cases (case 5). Mitotic activity or necrosis was not identified.

DISCUSSION

PMX is a benign neoplasm of hair matrix and presents as a firm, slow-growing subepidermal/subdermal nodule typically found in the head and neck region.[910]

Woyke et al.[11] first described the cytological features of PMX in 1982. Since then, several reports primarily of case reports and short case series are available on the cytological features of PMX.[7] It causes a diagnostic challenge for cytopathologists. It is often misdiagnosed due to unawareness of the spectrum of cellular features seen in FNA.[12]

Characteristic features of PMX are basaloid cell clusters, shadow (ghost) cells, nucleated squamous cells, giant cells, and calcification.[9]

Although cellularity was rarely mentioned in previous publications, Lemos et al.[7] stated that high cellularity was observed in their nine case series as in our cases.

Basaloid cells are the predominant cell type as stated in different reports.[2671213] These cells are seen singly or in sheets.[12] They have small-medium-sized regular, round nuclei with fine, evenly dispersed chromatin. Some basaloid cells have large nucleoli.[7] Their cytoplasm is scant and has indistinct cell borders.[612] In our study, basaloid cells were prominent in all cases except one. Although these cells usually form cohesive groups, they were also scattered as single cells in three cases. Nucleoli was prominent in only one of the cases (case 6).

Viero et al.[1] detected the presence of a delicate, fibrillary, pink/red colored (MGG) material surrounding the basaloid cells in all of their cases and stated that it is a pathognomonic finding in the diagnosis of pmx along with others.

Squamous cells are mostly in anucleated ghost cell morphology, but may occasionally appear as dark, small-nucleated keratinized cells.[16712] Although their number was few, these cells were present in all our cases.

Shadow (ghost) cells usually occur in large sheets of pale, non-nucleated cells with distinct cell borders.[6] They can also appear as single cells. They often have a refractile quality on both Diff-quik and PAP-stained preparations.[5] Ghost cells were prominent in all of our cases.

It has been reported that foreign body type giant cells often accompany calcification foci, basaloid, and squamous cells.[67] These cells were observed in two of our cases and it was noted that these cells were close to basaloid cells.

Free-lying calcium deposits and calcifications were observed in all cases of Viero et al.[1] This finding was also present in the majority of the cases of Domanski et al. and half of the cases of Wang et al.[56] Calcium deposits were observed in only one of our cases.

The presence of inflammation and debris in the background is also frequently mentioned in previous publications.[167] Debris was present in all of our cases and accompanied by inflammation in four cases.

Necrosis was also not a common finding in previous publications.[2913] Lemos et al.[7] detected mitosis in one of their cases. Necrosis and mitosis were not observed in our cases either.

Cytological findings of PMX may show similarities with many benign and malignant tumors and non-tumor lesions. The most common situation that causes difficulty in diagnosis is the predominance of one of the cell components and the absence of others.

If the basaloid cell component is dominant, Merkel cell carcinoma (MCC), basal cell carcinoma (BCC), small round cell tumors, and salivary gland tumors containing basaloid cell components are included in the differential diagnosis.[6713]

Nuclear morphology is helpful in the differentiation of PMX from malignant tumors.[614]

The nuclei of the basaloid cells are regular and uniform and have fine granular chromatin patterns in PMX.[67]

In MCC, small and fragile tumor cells with nuclear molding and individual cell necrosis are prominent cytologic features.[1] BCC usually consists of tight, well-defined clusters of uniform basaloid cells without nucleoli.[6] Peripheral palisading and clusters with sharp borders are helpful to differentiate from PMX.[16] The nuclei in BCC are inconspicuous and giant cells, shadow cells are not featured. Mature squamous cells are rarely identified.[5] The basaloid cells of PMX may also resemble small round blue cell tumors. A previously reported case of PMX was diagnosed as a blue cell tumor due to the rosette-like appearance of basaloid cells.[15] Clinical correlation and ancillary tests are helpful to distinguish these lesions.[5] On FNA some salivary gland tumors are largely composed of basaloid cells like PMX but they also have a characteristic stroma that helps the diagnosis (e.g. pleomorphic adenoma and adenoid cystic carcinoma).[516]

In cases where the squamous cell component is predominant, squamous cell carcinoma (SCC) and inclusion cysts are included in the differential diagnosis.

In SCC, FNAs are characterized by atypical squamous cells showing pleomorphism and hyperchromasia.[1718] Furthermore, basaloid cells of PMX may be indistinguishable from those aspirated from poorly differentiated SCC and the distinction may be difficult.[19] A predominance of shadow cells may suggest a cytologic diagnosis of epidermal inclusion cyst (EIC) (e.g. case 4).[112] In ruptured EIC, the presence of foreign body granulomatous reaction with multinucleated giant cells may lead to misdiagnosis of PMX. The absence of basaloid cells and calcific debris are helpful in making the correct cytologic diagnosis.[5]

There are very few studies examining the features of PMXs on fine-needle aspiration biopsy (FNAB) and no studies showing their features on LBC slides. In our study, all cases had LBC slides. In cytopathological examination, we saw the same cytological features such as basaloid cells, squamous cells ± debris/shadow cells as in conventional smears.

In conclusion, excisional biopsy is often the preferred method of diagnosis for the cutaneous masses. FNAB of PMX can be a diagnostic challenge. There are very few reports on the cytologic features of PMX in FNAB smears. The presence of ghost cells and basaloid cells should suggest the possibility of PMX. The presence of giant cells, fibrillary matrix, calcium deposits, squamous cells, naked nuclei, inflammation, and debris are cytological findings supporting the diagnosis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.
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